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Waste and Biomass Valorization (2022) 13:2769–2793

https://doi.org/10.1007/s12649-021-01669-7

REVIEW

Sargassum Invasion in the Caribbean: An Opportunity for Coastal


Communities to Produce Bioenergy Based on Biorefinery—An
Overview
Catia Giovanna Lopresto1 · Rosy Paletta1 · Pierpaolo Filippelli2 · Luana Galluccio2 · Cinthia de la Rosa3 ·
Eurípides Amaro3 · Ulises Jáuregui‑Haza4 · J. Atilio de Frias3,5

Received: 7 June 2021 / Accepted: 15 December 2021 / Published online: 13 January 2022
© The Author(s), under exclusive licence to Springer Nature B.V. 2021

Abstract
Purpose Sargassum spp. is one of the most abundant brown macroalgae. Pelagic species of this genus are habitat to numer-
ous marine species, however, its recent blooms in the Caribbean have posed a serious problem for local communities.
Methods This comprehensive review focuses on pelagic Sargassum, its chemical composition and its importance for marine
ecosystems in contrast with its negative economic, ecological and health impacts during massive beaching events.
Results The valorization of macroalgae is widely discussed with focus on biogas production from Sargassum via anaerobic
digestion as well as the effect of pretreatment and biosorption of heavy metals on biogas yields.
Conclusion Local communities can use macroalgae as raw materials and manage processes to obtain biofuels by essential,
simple, flexible, and cheap tools for self-supply. In this review we discuss on Sargassum valorization from an energy stand-
point to compensate coastal communities affected by these beaching events to transform a problem into a solution.
Graphical Abstract

Keywords Sargassum · Caribbean · Anaerobic digestion · Valorization · Beaching events

Catia Giovanna Lopresto and RosyPaletta have contributed equally


to this manuscript as first authors. Statement of Novelty

* J. Atilio de Frias This review deals with the Sargassum blooms in Caribbean
atilio.defrias@ufhec.edu.do from a positive perspective to produce energy from free
1
Department of Computer Engineering, Modeling,
and abundant biomass. Anaerobic digestion is an attrac-
Electronics and Systems (DIMES), University of Calabria, tive waste treatment practice in which both pollution con-
Rende, Italy trol and energy recovery can be achieved. The anaerobic
2
Department of Mechanical, Energy and Management digestion, described in previews studies, was accurately
Engineering (DIMEG), University of Calabria, Rende, Italy reported together with the evaluation of the Biochemical
3
Universidad Federico Henriquez y Carvajal (UFHEC), Methane Potential (BMP). In addition, adequate pretreat-
Santo Domingo, Dominican Republic ments and co-digestions of Sargassum with other biomasses
4
Instituto Tecnologico de Santo Domingo (INTEC), were extensively reported to enhance methane yields and
Santo Domingo, Dominican Republic make the process more cost-effective, as well as the addi-
5
Av. Máximo Gómez esq. César Nicolás Penson, tion of nanoparticles. Consequently, this review presents an
Santo Domingo, Dominican Republic

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Vol.:(0123456789)
2770 Waste and Biomass Valorization (2022) 13:2769–2793

updated and extensive overview of Sargassum exploitation Unprecedented Sargassum Influx in the Gulf
by anaerobic digestion, with a focus on persisting drawbacks of Mexico
and future challenges.
The Gulf of Mexico and the Sargasso Sea have the largest
concentration of pelagic Sargassum (S. natans and S. fluitans
Introduction [22]) in the world [23]. The seasonal blooms of Sargassum
are investigated in the tropical and subtropical North Atlan-
Floating Sargassum: General Information tic [24] with spatial and temporal distributions. Floating Sar-
gassum in the western Gulf of Mexico was observed from
Marine macroalgae or seaweeds are multicellular plants with space in 2005 for the first time [25]. Sargassum moves from
a very complex diversity and composition. Based mainly the Sargasso Sea through the Caribbean Sea and into the
on their photosynthetic pigments and morphology, they are Gulf of Mexico, promoted by the Azores high-pressure sys-
classified into three main groups: brown algae (Phaeophy- tem [26]. Satellite images from the European Space Agency
ceae), red algae (Rhodophyceae) and green algae (Cholo- show a seasonal cycle in North Atlantic and Gulf of Mexico,
phyta) [1]. with peak blooms between March and September [5].
Brown algae are the most complex algal organisms, with Until 2010, Sargassum originated in the northwest Gulf
a unique mechanism of photon absorption during photosyn- of Mexico in the spring of each year, and then it moved to
thesis [1]. The predominant brown color is a result of carot- the Atlantic Ocean, ending in the northeastern Bahamas in
enoids (i.e., fucoxanthin) [2]. Among the 2000 species of February of the following year [23, 27]. Nevertheless, an
brown alga, Sargassum or ‘Sargasso’, as is known colloqui- unprecedented floating Sargassum outbreak formed lines
ally, is the most abundant [3]. The name originated from its stretching from West Africa to the Caribbean Sea in 2011
presence in the Sargasso Sea, first reported by Christopher [28, 29]. Satellite images suggested a new Sargassum ori-
Columbus in the fifteenth century [4, 5]. gin region [21], further south than the previous one. This
Floating Sargassum in open sea is an essential habitat for new area of algal masses was named the Great Atlantic
several marine species, providing food, refuge, and breeding ‘Sargasso’ Belt and consisted of 8850 km in the Atlantic
grounds for fishes, sea turtles, marine birds, crabs, shrimp, Ocean corresponding to 20 million metric tons [5]. Sargas-
and more [6]. Some animals, like the Sargassum fish or frog- sum blooms arise in an area identified as the North Equa-
fish, live their whole lives only in this habitat. A synergistic torial Recirculation Region (NERR) [30, 31], north of the
relationship between Sargassum and fishes contribute to mouth of the Amazon along the northern coast of Brazil in
nutrient supply and growth in nutrient-poor waters of the the western Equatorial Atlantic [32–34]. Such distributions
Sargasso Sea [7]. had not been seen previously in the tropical Atlantic and
Some species of Sargassum also serve as feedstock for could be explained by nutrient supply in that region, chang-
value-added products by the agro-food, textile, cosmetic and ing weather conditions and anomalous winds [35]. These
pharmaceutical industries, especially in Asian countries [2, extraordinary beaching events peak during the spring and
6, 8, 9]. In addition, high-value functional compounds can be summer months and have worsened in recent years.
extracted from Sargassum species, such as polyunsaturated The accumulation of Sargassum in the Caribbean Sea
fatty acids [10], sulfated polysaccharides and polyphenols and Central Atlantic Ocean in the years 2015, 2018, 2019
with antioxidant, antiproliferative and other therapeutic 2020 and 2021, is shown in Fig. 1. This figure is based on
activities [11–15]. A very recent application concerns the data extracted from the monthly bulletins published by the
formulation of alginate-based edible film from Sargassum University of South Florida Optical Oceanography Labora-
fluitans incorporated with silver nanoparticles synthesized tory [36] and data from literature [5, 35].
by a green method [16]. Since the first significant Sargassum bloom in 2011,
Nevertheless, excessive amounts of Sargassum on the years 2015 and 2018 experienced the largest Sargas-
beaches in populated areas can cause problems. Even though sum buildup ever recorded during the peak months between
the cause of excessive blooming in recent years has not been March and September [5, 35]. The large presence of Sargas-
defined, it may be a result of large-scale atmospheric and sum in 2015 may be a result of higher nutrient availability in
oceanic forcing, related to increasing water temperatures, spring and early summer from the central east Atlantic and
climate change and weather fluctuations [6, 17, 18]. Moreo- Amazon River, maybe caused by increased deforestation and
ver, human modification of biogeochemical cycles, result- fertilizer use in Brazil, and increased water-column nitro-
ing in ocean acidification and eutrophication, due to high gen with time and for the highest water temperature in this
amounts of nutrients from rivers, agricultural fertilizers and period of the year [5]. In the next few years, the continuous
wastewater from cities, could contribute to the proliferation nutrient flow, as well as climate change, are consistent with
of Sargassum in recent years [19–21].

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Waste and Biomass Valorization (2022) 13:2769–2793 2771

Mean Sargassum biomass per month (million 25 ammonium, phosphorus and sulfide [45–47]. The coastal
accumulation can form a one-meter high “wall”, precluding
20 access to nesting sites for turtles and creating a contami-
nated incubation environment [48]. Moreover, the accumu-
15
lated Sargassum may also cause beach erosion, depending
metric tons)

on local conditions [20]. Finally, Sargassum breaks down


10
rapidly on beaches with emission of harmful gases [17, 45]
causing respiratory problems, particularly for asthmatics
5
[49].
0
Massive Sargassum beaching events are recent phe-
March April May June July August September nomena for many residents in the Caribbean, who feel the
2015 2018 2019 2020 2021
socio-economic impacts of such influx [43]. The removal of
Sargassum from beaches or the prevention of it reaching the
beaches can be very expensive, with a cost of around US$
Fig. 1  Sargassum spp. accumulation in the Caribbean Sea and Cen-
tral Atlantic Ocean (5° S–25 ºN, 89° W–15° E) during the peak 5 million on the Mexican Gulf of Mexico and an estimated
bloom months between March and September in the years 2015, cost across the Caribbean of US$ 120 million [50]. The Car-
2018, 2019, 2020, 2021. Data were not available for May 2021 (data ibbean Regional Fisheries Mechanism has even estimated
from [5, 35, 36])
the clean-up costs of Sargassum for the Caribbean beaches
in 2018 at $ 210 million [21]. Caribbean communities have
the peak accumulation recorded for the region in the month not yet found sustainable solutions to remove the excess of
of June 2018, at 20.4 million metric tons [37]. The Sargas- Sargassum from coasts to preserve the ecosystems and the
sum accumulation in 2019, 2020 and 2021 (Figs. 1 and 2) tourism industry. Indeed, Sargassum blooms can last for
seems to support the observations by Wang et al. [5], and weeks at a time and negatively affect tourism-based econo-
Sargassum blooms and beaching events may be a recurring mies of the coastal regions [6]. The current remediation to
phenomenon over time. minimize its impact consists in the manual or mechanical
Floating algae density, in terms of percentage of area cov- collection of Sargassum, preferably within 72 h of arrival
ered [38], was daily monitored during 2020 [36], using the [20], followed by landfills disposal [42]. Nonetheless, inad-
Moderate Resolution Imaging Spectroradiometer (MODIS) equate disposal of Sargassum contaminate aquifers with
[18, 39]. Recently, the surface area covered by floating Sar- nutrients, salt, metals and other contaminants [20]. Recently,
gassum in the Northern Mexican Caribbean during Sargas- some authors highlighted the importance to develop suc-
sum influx in September 2018 was evaluated through the cessful strategies by an interdisciplinary approach from
analysis of multispectral images and supervised by machine exploration to management by including detection, collec-
learning approach [40]. Density is calculated as a mean of tion, stabilization, and experimentation [43]. Nevertheless,
the past 7 days, and based on the corresponding Alterna- no official information are available to identify the specific
tive Floating Algae Index (AFAI) images using the method role of local communities in the different phases.
described by Wang and Hu [18]. In Fig. 2 we summarized The cause, effects, and potential solutions of the outbreak
the monthly monitoring of the floating algae density in the are topics of international debate [51]. The Ministry of Envi-
Eastern Caribbean. In 2020 blooms occurred during the ronment and Natural Resources of Dominican Republic esti-
spring and summer months, from April to September. mated that 49 national beaches in the country were impacted
by the arrival of Sargassum in 2018, with an accumulation of
Adverse Impacts of Massive Sargassum Influx 2,424,800 cubic meters [52]. Consequently, the approach of
sustainable and scientific solutions to overcome the impact
Recent studies have shown that Sargassum invasions affect of Sargassum on ecosystems, fishery and tourism is essential
coast and beach ecosystems [41, 42]. A very recent work for the Dominican reality. This unprecedented invasion may
highlighted the adverse ecological impacts of Sargassum deliver several economic opportunities in the energy sector
influx, in terms of coastal impacts, fauna, ecosystems and [53, 54].
biodiversity [43]. Sargassum decomposition creates Golden
or Brown Tides, turning water brown and blocking sunlight Sargassum as a Resource for a Bioenergy Strategy
penetration with consequent anoxic conditions, loss of nutri-
ents and production of toxic gases [42, 44]. Consequently, Bioenergy from renewable biomass resources is an impor-
coral species, seagrass, benthic communities and fauna spe- tant alternative to traditional fossil-derived energy, con-
cies die in greater proportions than previous times, due to tributing to the final energy demand for different needs,
low concentration of dissolved oxygen and high values of especially cooking and heating. Identifying the reasonable

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2772 Waste and Biomass Valorization (2022) 13:2769–2793

Fig. 2  Monthly monitoring of floating algal density in the Eastern Caribbean, an area bounded within these coordinates: 23° N 10° N 60° W and
75° W [36]. The highlighted areas are Sargassum blooms

cultivation locations, appropriate bioenergy crop types, Nevertheless, first- and second-generation bioenergy
and optimal management practices can be beneficial to from agricultural or dedicated crops without comple-
environment and sustainable development of bioenergy. mentary measures showed evident food/feed vs. fuel

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Waste and Biomass Valorization (2022) 13:2769–2793 2773

competition and environmental impacts in terms of water Characteristics of Sargassum


issues, greenhouse gas emissions (due to deforestation, as
an example), use of fertilizers, soil organic carbon, soil Described for the first time 200 years ago [8], Sargassum
erosion and biodiversity [55–58]. Even the conversion of is a genus of brown macroalgae. It belongs to the family
marginal low-productive lands [59] and semi-arid or arid Sargassaceae, order Fucales, class Phaeophyceae, subclass
areas [60] is not sustainable on a large scale, as well as Cyclosporeae, phylum Heterokontophyta [2]. It has a typical
the exploitation of perennial energy crops on degraded brown color due to the presence of xanthophylls, a class of
soils suffers of lack of sufficient information [61]. The oxygen-containing carotenoids. The main pigment in Sar-
bioenergy production from microalgae has been described gassum is fucoxanthin.
as a promising strategy during last decades [62, 63], but, Sargassum is morphologically one of the most complex
also in this case, the economic feasibility on commercial phaeophycea [8]. It is composed of many leafy appendages,
scale and the environmental sustainability are still far branches, and round, berry-like gas-filled structures called
from being reached [64]. Despite many challenges and pneumatocysts. Pneumatocysts add buoyancy to the plant
critical bottlenecks, bioenergy can contribute to energy structure and allow it to float on the water surface. The larg-
security in countries and support them in meeting their est members can reach several meters in length. The Sargas-
national goal in terms of poverty reduction, improved sum thallus, shape of the leaves, basis of the leaves, pedicel,
health and wellbeing and climate action. For this reason, leaves margin, midrib and apex vary from species to species
bioenergy-based strategies and encouraging policies have [2].
been introduced from many countries, to achieve multiple About 150 species are distributed worldwide throughout
aims: mitigation of climate change on a global scale [65]; temperate and tropical seas [12]. Pelagic species of Sargas-
making people independent in biofuel production and tak- sum were the main component ranging from 78.1 to 99.6%
ing advantages of wastes destined to expensive disposal of the total beach-cast fresh biomass in the north coast of
on a local level [66]. the Mexican Caribbean [40]. Thus, the most common spe-
cies in the Caribbean Sea are the free-floating Sargassum
Aims and Objectives fluitans and Sargassum natans [5, 6, 30, 68]. These are the
only two holopelagic Sargassum species that spend their
This review paper provides a comprehensive updated whole life cycle in the water surface [69]. Each species has
overview of the morphological characteristics of Sargas- distinct morphological forms. In particular, scientists identi-
sum, its chemical composition, with a focus on produc- fied two morphological forms of S. fluitans (III, X) and four
tion of biogas by anaerobic digestion. Indeed, Sargassum forms of S. natans (I, II, VIII, IX) [28]. Both species are
is a renewable, abundant biodegradable biomass, and a characterized by several blades, highly branched thalli, and
potential feedstock for energy production. Thus, the aim pneumatocysts, creating a floating biomass in the ocean sur-
of this work is to disclose recent advances in the valoriza- face [7]. They reproduce asexually by fragmentation of thal-
tion efforts of the massive Sargassum influx, based on the lus. Light, nutrients and warm temperatures promote their
pretreatment of feedstocks and the production of biogas to growth and oceans are their ideal habitat. Photosynthesis
meet local energy demands. Small island developing states occurs when Sargassum is on the water surface, and when
in the Caribbean face serious challenges relating to waste this alga decompose on shores, its color become dark brown
management, sewage treatment, and energy sustainability, and toxic gases are emitted [70].
but inefficient and poorly planned delivery of these key ser-
vices has a negative impact on the quality of people’s lives
and the environment. Action across the public and private Chemical Composition of Sargassum
sector is needed to address these issues in a cost-effective,
controlled and sustainable manner [67]. Small-scale plants The chemical composition of Sargassum is very complex
have many social, economic and environmental advantages and varies from one species to another, in addition to the
and significantly contribute to renewable energy production spatial and temporal variations among the same species.
and local development [66]. Communities can use/reuse This phenomenon is probably a result of different algae
local raw materials and manage independently processes growth across seasons [9]. The spatial and temporal vari-
to obtain biofuels by essential, simple, flexible and cheap ations in the chemical composition of Sargassum, need to
tools for self-supply. be understood in order to develop preservation techniques
Therefore, the creation of a circular economy could miti- during Sargassum bloom and ensure an eventual consistent
gate damage to the environment and coastal communities. supply of value-added products [6].

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2774 Waste and Biomass Valorization (2022) 13:2769–2793

The most abundant components are carbohydrates and the form of ammonium ion, whose high level increases the
ash, while the content of lipids and fibers is low [50, 71]. pH in the digester and is toxic for methanogens bacteria [72].
Moisture content is generally high, ranging from 70 to 90%, To attain a stable digestion process, the optimal C:N ratio of
whereas ash content (dry basis) ranges from 10 to 76%. The substrate is suggested in the range of 20–30 [72]. It is evi-
main disadvantages associated with such high moisture val- dent that C/N of pelagic Sargassum varies with season and
ues are the use of limited organic loading rates of the digest- harvest site, ranging from 7 to 14 in China to around 22–27
ers, and the short period of biomass storage [72]. in the Caribbean. Due to its oceanic growth conditions, mac-
Sargassum has a high capacity to absorb metals and other roalgae contain high level of salts with a negative effect on
elements, included toxic metals that may leach into ground- biogas production [6]. Macronutrients (Na, Mg, Al, P, K and
water. These metals have been detected in samples of S. flui- Ca) are essential for anaerobic growth, metabolic activity
tans and S. natans on Mexican and Dominican shores: Al, and biodigester stability [75], but high salt level cause bacte-
As, Ca, Cl, Cu, Fe, K, Mg, Mn, Mo, P, Pb, Rb, S, Si, Sr, Th, rial cells to dehydrate due to osmotic pressure, slow down
U, V, Zn. Arsenic concentration ranges from 24 to 172 ppm the growth and can cause severe inhibition or toxicity [83].
[73–75] and should be specially monitored for its possible In addition, high Na content influences bacterial archaeal
toxic effects above certain limits. communities. Indeed, a sodium concentration of 4.42 g L ­ −1
Bioactive compounds, such as flavonoids, saponins, tan- promoted the growth of Paludibacter and Fibrobacter while
nins, phenolics, alkaloids, terpenoids, and cardiac gluco- a sodium concentration of 20.15 g L ­ −1 inhibited the aceto-
sides, were also detected [76]. clastic methanogen growth in the anaerobic digestion [81].
Diversity in chemical composition of red, green and Moreover, microorganisms require traces of microelements
brown macroalgae was recently studied [77]. The pro- (Fe, Ni, Zn, Cu) for their growth and methane production,
tein, lipid, carbohydrate, and ash content were reported but the accumulation of As, Cd, Cr, Hg and Pb is toxic, as
in the ranges of 5.8–14.1%, 0.6–2.7%, 13.4–46.1%, and well as the presence of carbamates [80]. Pelagic Sargassum
24.6–76.4%, respectively. can contain a large amount of heavy metals; Fe > Mn > Zn
Other authors recently reported a compositional analysis > As > Ni > V > Cu > Cr > Co > Hg > Cd > Pb, which
of mixed Sargassum and the individual species S. natans have a negative impact on anaerobic digestion after their
VIII, S. natans I, and S. fluitans collected in Turks and Cai- release from the feedstock [75]. The toxic effect of heavy
cos in 2019 [50]. All samples showed high moisture con- metals is due to disruption of enzyme function and structure
tent (82–87%) and ash content (34–47% dw). Ash was rich by binding of the metals with thiol and other groups on pro-
in sodium chloride and salt concentration was 2.6–2.9% tein molecules or by replacing naturally occurring metals in
weight. Heavy metals, phenols, sulfur, carbon, proteins, fib- enzyme prosthetic groups [83].
ers, and lipids were also analyzed [50]. The same species, With regard to the proximate composition, insoluble
collected in the north coast of the Mexican Caribbean dur- fibres are recalcitrant to anaerobic digestion and polyphenols
ing the Sargassum influx in September 2018, were recently are inhibitors for anaerobic digestion [84]. The theoretical
characterized. Chemical composition resulted to be spatially yields of methane from lipids, proteins and carbohydrates
homogeneous for most of the components analyzed, and are 1.014, 0.851, and 0.415 ­LCH4 ­g−1 VS (Volatile Solids),
scarce differences were observed only for some inorganic respectively [72]. Therefore, lipids give the highest theoreti-
components such as ash, elemental carbon and metal content cal yield, but their level in Sargassum is very low.
[40].
In addition, the proximate and elemental composition,
as well as physico-chemical characteristics of pelagic Sar- Use of Sargassum as a Source of Energy
gassum collected from waters in Barbados in 2018, were
analyzed [75]. Its content of micronutrients, macronutrients The growing accumulation of Sargassum on Atlantic coast-
and trace elements was also determined. lines has raised awareness in the scientific community about
Table 1 summarizes the chemical composition of pelagic the potential sustainable use of this macroalga as a source
Sargassum biomass according to different studies. of energy and value-added products, to restore beach shores
The chemical composition of macroalgae is very impor- and promote the growth of the tourism and fishing sectors
tant and influences the anaerobic digestion to produce biogas [6]. Sargassum may be a more sustainable energy source
when macroalgae are used a substrate. The concentration than terrestrial crops because it does not need land for their
of carbon and nitrogen is critical, because the carbon-to- growth [85], and biofuel production is one of the most
nitrogen (C/N) ratio strongly affects the AD process. When researched applications [86].
C/N is very high, nitrogen consumption happens quickly and Anaerobic digestion (AD) consists of the anoxic degrada-
biogas production decreases [80]. On the contrary, a low tion of organic matter, a key biological process for convert-
C/N ratio cause the release and accumulation of nitrogen in ing biomass into energy and for the valorization of waste as

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Waste and Biomass Valorization (2022) 13:2769–2793 2775

feedstock. The main product of AD is biogas (60% meth- Physicochemical Pretreatments


ane), which can be used as biofuel or as a thermal energy
source [87]. The Biochemical Methane Potential (BMP) is Physicochemical pretreatments combine physical and chemi-
the optimal amount of methane that an organic matrix can cal methods by treating the biomass with or without a chemi-
produce via AD. Different pretreatment methods for bio- cal under high temperature and pressure. Some techniques
mass disruption, such as mechanical, thermal, enzymatic, include a rapid decompression step (e.g. steam explosion,
and thermo-chemical treatment, have been shown to success- ammonia fiber expansion (AFEX), C ­ O2 explosion, thermo-
fully improve biomethane recovery. Additionally, co-diges- chemical treatments, hydrothermolysis, supercritical flu-
tion trials of seaweeds mixed with other wastes improved the ids) [86, 89]. These pretreatments are effective for biomass
overall quality of biomass conversion. decrystallization and for increasing the surface area [89, 96].
The AFEX method is like steam explosion, with the excep-
Pretreatments of Macroalgae tion that biomass is exposed to liquid ammonia for a period
prior to decompression. As opposed to steam explosion, the
A key aspect in the optimization of AD performance from ammonia pretreatment has the advantage of producing no
macroalgae is the pretreatment. This process involves the fermentation inhibitors and eliminating the need of a water
physical, biological, chemical or physicochemical decon- wash [97]. On the other hand, hydrothermal pretreatment
struction of the cell wall matrix to remove or alter the is considered an eco-friendly technology compatible for
structures of hemicellulose and lignin (if present), and to Sargassum. It enhances the bioavailability of organics for
preserve the cellulose fraction [88, 89]. This facilitates the digestion with the advantage that it does not need prelimi-
hydrolysis of cellulose to glucose. Moreover, the methano- nary drying of algae [92, 98]. Additionally, it mitigates the
genic potential of brown algae depends on the breakdown presence of hydrogen sulfur in biogas [99] and enhances the
of carbohydrate chains, with alginate being the most abun- properties of the digestate, yielding high-quality bio-ferti-
dant carbohydrate [90]. Macroalgae have little or no lignin, liser or soil conditioner with agricultural application [75].
therefore they are less recalcitrant than other lignocellulosic Other physicochemical pretreatments include autohy-
biomasses. Nonetheless, brown seaweeds are more recalci- drolysis, liquid hot water and autoclaving, which are effec-
trant to digestion compared to red and green seaweeds [91]. tive at breaking the fiber structures of biomass to isolate its
A useful classification of seaweed pretreatment was reported fundamental sugar units which can be converted into biogas
in literature [86, 92]. [94, 100].
Before pretreatment, macroalgae should be washed Even though high temperatures promote biomass solubili-
and dried. Even though washing removes all inert materi- zation and extraction, one disadvantage is that temperatures
als (e.g. stones, sand, salts) and frees the organic matrix, higher than 180 °C lead to the formation of inhibitory com-
increased biogas yields downstream depend on the pretreat- pounds such as furfural, hydroxymethylfurfural and phenols
ment process [93]. After the washing step, moderate dry- that are inhibiting for bioconversion [92]. Hydrothermal or
ing increases sample stability, decreases processing volume pressurized hot water (110–180 °C, 6–25 bar) pretreatment
and decreases moisture content. However, excessive drying work at relatively lower temperatures and yield lower inhibi-
of the organic matrix reduces the surface area available for tory compounds.
effective enzymatic hydrolysis prior to biogas production
[94]. Previous studies have reported that excessive drying Biological Pretreatments
of biomass, before or after pretreatment, causes a reduc-
tion of its pores and irreversible collapse, which lowers Biological pretreatments are based on natural microorgan-
the amount of glucose that can be released by enzymatic isms that degrade lignin and hemicellulose in biomass, such
hydrolysis [95]. as fungi, bacteria, and enzymes. White rot fungi extracted
from decaying wood are the most promising microbes used
Physical Pretreatments in biological pretreatment [92]. A macroalgae isolated from
the Mexican Caribbean was pretreated with a Bm-2 strain
Mechanical pretreatments reduce the size of biomass par- (Trametes hirsuta), producing a 20% higher methane yield
ticles down to 0.2–2 mm to decrease cellulose crystallin- [101]. However, these biological methods are limited by
ity [94], increase the reaction surface to volume ratio and long reaction times and low hydrolysis rates. [89, 102].
increase accessibility to complex sugars. Despite the effec-
tiveness of physical pretreatments, the practicability of these Chemical Pretreatments
methods is limited because energy consumption can be high
[89]. Chemical pretreatments are generally more effective at
removing lignin and/or hemicellulose and exposing the

13
Table 1  Proximate and elemental composition of dried biomass from pelagic Sargassum inundations
2776

Site and year of Nigeria Dominican Ghana Trinidad Barbados Mexican Carib- Mexican Carib- Cancun, Mexico Turks and Caicos China China
collection (2012) [76] Republic (2015) [78] and Tobago (2018) [75] bean bean (2019) [80] (2019) [50] [81] [82]

13
(2015) [73] (2017) (2018) [40] (2018–2019) [74]
[79]

Moisture (%) 9.0 ± 0.14 18.9 ± 0.05 20.63 ± 0.93 83–86 81.98–87.41
(on fresh bio- (on fresh bio-
mass) mass)
Ash (%) 8.65 ± 0.07 13.43 ± 0.01 31.82 ± 1.34 18.1–23.9 33.63–46.94 19.40
Proximate analysis
Protein (%) 15.4 ± 0.0 4.7 ± 0.23 8.1–10.3 2.99–4.19
Lipids (%) 2.5 ± 0.07 0.01 ± 0.00 2.5–3.4 3.58–4.56
Carbohydrates 57.3 ± 0.21 63.1 ± 0.06 14.0–17.0 11.68–27.40
(%)
Crude fibre (%) 7.15 ± 0.21 31.15–37.41
Elemental analysis
Ag (ppm) < 0.6
Al (ppm) 303–4188 2300.08 ± 57.73 < 140–517 0.032 16.21–37.5
As (ppm) 13.7–42.3 13–53.5 35.22 ± 0.61 29.0–65.7 24–172 20.94–123.69
B (ppm) 10,224–
116,294
Ba (ppm) 6.8–16.5 < 36 0.243
Be (ppm) 0.006–0.053
C (%) 27.50 ± 0.65 (%TS a) 26.8–33.0 28.8 27.41–29.23 19.40 25.9
Ca (ppm) 96,901– 48,895.20 ± 1232.16 23,723–136,146 539.5 26,020–70,306
133,400
Cd (ppm) 0.1–0.3 78–119 0.79 ± 0.01 0.32–1.36 <2 0.09–0.13
Ce (ppm) 0.4–3.2
Cl (ppm) 22.5–1353 747–53,101
Co (ppm) 0.4–1.1 6.51 ± 0.15 < 11
Cr (ppm) 2.3–55.5 12.96 ± 0.39 <8 0.011 < 0.43
Cu (ppm) 1.6–11.9 24–36 25.08 ± 0.59 < 0.20–1.09 < 6–540 0.036 1.25–2.91
Fe (ppm) 8700 ± 280 20–655 1209–5910 2398.37 ± 52.52 24.0–54.6 < 3–11 0.251 81.58–3811
H (%) 4.16 ± 0.30 (%TS a) 3.4 3.13–3.7 5.57
Hg (ppm) 0.5–1.4 1–2 1.36 ± 0.04 < 0.01
I (ppm) 40 ± 0 <1
K (ppm) 28,000 ± 740 2208–33,602 0.72–2.48 49,973.09 ± 1179.36 1990–46,002 7444–69,359
Mg (ppm) 42,755 ± 350 10,211– 8233.78 ± 170.44 < 2915–13,662 75.267 12,053–16,547
18,240
Mn (ppm) 15.6–32.2 337.51 ± 7.93 40–139 0.156 < 3–30.15
Waste and Biomass Valorization (2022) 13:2769–2793
Table 1  (continued)
Site and year of Nigeria Dominican Ghana Trinidad Barbados Mexican Carib- Mexican Carib- Cancun, Mexico Turks and Caicos China China
collection (2012) [76] Republic (2015) [78] and Tobago (2018) [75] bean bean (2019) [80] (2019) [50] [81] [82]
(2015) [73] (2017) (2018) [40] (2018–2019) [74]
[79]

Mo (ppm) 0.6–3 < 1–7


N (ppm) 6360 ± 200 0.62–1.04 1.21 ± 0.06 (%TS a) 9000–11,000 1.2 (%) 1.28–1.71 (%) 1.38 (%) 3.58 (%)
Na (ppm) 3802–21,068 14,890.65 ± 288.88
Ni (ppm) 10–32.5 34.90 ± 0.90 < 10
O (%) 34.49 ± 0.18 (%TS a) 39.7 20.62–31.79 24.18
P (ppm) 96,500 ± 21,200 761–1145 855.13 ± 11.89 228–401 138.3–500.6
Pb (ppm) 1–2 86–335 0.40 ± 0.01 < 0.20–0.29 < 2–3 0.26–0.48
Rb (ppm) 0.3–10.2 30–143
S (ppm) 60.2–70.3 0.82 ± 0.22 (%TS a) 9462–24,773 0.00–0.40 (%) 0.54 (%) 1.22 (%)
Waste and Biomass Valorization (2022) 13:2769–2793

Se (ppm) < 0.0001


Si (ppm) 0.25–0.72 447–2922
Sr (ppm) 1162–1436 1605–2564
Th (ppm) 0.04–0.43 5–23
Ti (ppm) < 29
U (ppm) 37.3–91.7 11–48
V (ppm) 1.1–2.8 25.76 ± 0.64 < 3–13
Zn (ppm) 50 ± 0 12.7–20.6 16–100 105.65 ± 2.16 3.6–7.2 < 5–17 0.098 5.81–35.64
Zr (ppm) 7.6–38.2 <2
a
TS: total solids (79.30 ± 0.93 wt.%)

13
2777
2778 Waste and Biomass Valorization (2022) 13:2769–2793

cellulose fraction. These methods include alkalis, perox- compounds [114] and sea salts. The hydrolytic, acidogenic,
ides, Brønsted acids, organosolv (organic solvent + inor- acetogenic and hydrogenotrophic methanogenic bacteria
ganic acid), ozone, ionic liquids, and deep eutectic solvents are typically metabolized at different salinities, but aceto-
[86, 89, 103, 104]. clastic methanogens were severely inhibited at high saline
Alkali pretreatments use mild temperatures (< 160 °C) conditions. The acclimation of the inoculum at seawater
but longer times (hours to weeks) and follow a saponification concentrations could overcome this problem [115]. The
mechanism of intermolecular ester bonds crosslinking hemi- optimal C:N ratio for anaerobic digestion seems to be spe-
cellulose and lignin to remove both biopolymers [97]. In cies dependent [112]. Biogas yield also depend on a wide
dilute acid pretreatments, hemicellulose can be completely range of other variables such as inoculum, temperature,
removed from biomass at high temperatures (160–220 °C) reactor configuration and feedstock composition. Seasonal
and short times (< 30 min) following irreversible first-order and geographical biochemical variations were observed
kinetics in the hydrolysis to xylose. Organosolv can fraction- with consequent change in fermentable solids and meth-
ate biomass into solid lignin, solid cellulose fibers and an ane production [85]. Even different segments of seaweeds
aqueous hemicellulose stream [103]. Finally, ionic liquids showed significant variation in biochemical composition
degrade biomass by dissolving cellulose and/or removing and methane potential [116]. Temperature strongly influ-
lignin via ionic, π–π, and hydrogen bonding interactions ences AD [117] and the best results were obtained at
[104, 105]. 35–37 °C. In addition, the volatile solid concentration of
seaweeds strongly affects the methane yield. Montingelli
Comparison of Pretreatments Techniques et al. [118] found that at the longest pretreatment time
(15 min) Laminaria sp. produced the highest methane yield
Other pretreatments outside of the aforementioned classi- (240 ­LCH4 ­kgVS−1) at the intermediate tested VS concen-
fications include ultrasonication [86], and microwave [92]. tration (2.5%), while A. nodosum showed the best yield
Overall, all pretreatment methods have advantages and dis- (169 ­LCH4 ­kgVS−1) at the minimum tested VS concentra-
advantages that must be considered at the laboratory, pilot, tion (1%). Finally, the inoculum source had a significant
or industrial scales (Table 2). impact on AD because of different bacterial communities.
Even though pretreatments may increase biogas yields, Anaerobically digested sewage sludge seemed effective
they require high-energy inputs, and it is difficult to achieve as inoculum for start-up of various substrates including
a positive net energy balance. For this reason, it is necessary seaweeds [119]. Batch anaerobic digestion is the simplest
to investigate the energy assessment of pretreatments [92] and most common configuration used worldwide. The main
in terms of Energy Return Over Investment (EROI) [106]. macroalgae species studied for AD methane production in
The energy required during pretreatments has been studied laboratory batch reactors during the last decade are pre-
for different techniques [107–109]. sented in Table 3.
For instance, hydrothermal pretreatment is a very promis- In some studies, AD seemed to be successful even with-
ing method for brown algae, since it improves methane yield out pretreatments, washing or removal of epiphytes [144].
with a net positive energy balance [92]. After 25 days, no significant improvement was recorded by
mechanical pretreatment with respect to the untreated Lami-
Production of Biogas by Anaerobic Digestion naria spp. [87]. Ball milling on dry samples and microwave
of Macroalgae pretreatment on wet samples decreased the methane yield
when compared to untreated macroalgae. Otherwise, pre-
The use of macroalgae as feedstock in bioenergy received treatments improved AD in most studies.
intensive scrutiny for the first time as part of the US Ocean Nielsen et al. [140] investigated the effect of mechani-
Food and Energy Farm project as proposed by Wilcox cal maceration pretreatment and observed that it increased
[110]. methane yield by 68% (U. lactuca), 17% (C. linum) and
Biogas production using algal biomass has been widely 11% (G. vermiculophylla). AD of chopped and wet U. lac-
studied as a green and alternative renewable technology tuca seems promising and more efficient than biomass pre-
[111]. Recent advances in biogas production by anaerobic treated in other ways [142]. Mechanical pretreatment was
digestion (AD) of macroalgae were extensively described also effective on F. serratus, F. vesiculosus Linnaeus, G.
[112] with a focus on pretreatments, operational and envi- gracilis, L. digitata, and P. caniculata, increasing biogas
ronmental parameters, future challenges and prospects for yield 182%, 222%, 110%, 51%, and 179%, respectively,
scaled-up applications [96, 99, 113]. One critical aspect of compared to untreated biomass [122]. Beating is frequently
AD of marine macroalgae in the inhibition by halogenated used in mechanical pretreatment on seaweeds, performing

13
Waste and Biomass Valorization (2022) 13:2769–2793 2779

two main actions: cutting and high-pressure beating. Beat- The enzymatic, acid, and combined pretreatments of L.
ing is suitable for wet or dry biomass, and a previous work digitata did not improve significantly biogas yields. Cel-
has reported a 37% increase in methane yields compared to lulase was the most effective enzyme, but it resulted in a
untreated biomass [118]. biogas yield of 232 L ­kgVS−1 that was very close to results
Microwave pretreatment dehydrates seaweed based on from untreated samples (228 L k­ gVS−1). Pretreatment with
irradiation, increasing biogas yields from AD with much alginate lyase was irrelevant (225 L∙kgVS− 1), whereas the
shorter residence times compared to other pretreatment commercial Celluclast® drastically reduced the biogas yield
methods [118]. A microwave pretreatment and its com- (72 L ­kgVS−1). Among organic acids, pretreatment with
bination with F ­ e3O4 nanoparticles (acting as a heteroge- 2.5% citric acid was the most effective (237 L ­ biogas ­kgVS−1),
neous catalyst) enhanced biogas yields from green algae whereas 1% oxalic acid, 1% lactic acid, 6% oxalic acid, 6%
as compared to individual ones and control [146]. The lactic acid and 6% citric acid reduced biogas yields (169 L
ultrasonic pretreatment, microwave, and ultrasonic pre- ­kgVS−1, 161 L ­kgVS− , 83 L ­kgVS−1, 101 L ­kgVS−1, and 69 L
treatment combined with microwave improved methane ­kgVS−1, respectively) compared to untreated samples. Even
yields by 67, 56, and 85%, respectively, when compared the combination of enzymatic and acid pretreatment did not
with the mechanical pretreatment of F. vesiculosus and F. improve significantly the biogas yield [130].
serratus [127]. Semi-continuous and continuously stirred tank reactors
Hydrothermal pretreatment of seaweeds increased biogas have been used to study AD of macroalgae, but there is no
yields, compared to untreated samples [98, 147]. Steam consensus in regards to their advantage over batch systems
explosion of S. latissima increased methane yield up to 20% [112, 138]. Few pilot-scale studies were also published [133,
[139]. Methane yields from S. latissima also increased after 148].
hydrotermal pretreatment in a two-stage process consisting
of a dark fermentation to produce biohydrogen followed by Anaerobic Digestion of Sargassum
anaerobic digestion [137]. On the other hand, thermal pre-
treatments did not improve AD for U. lactuca [142] and The BMP of brown algae is in the range of 204–380 L ­kg−1
P. palmata [145]. Also thermochemical pretreatment of L. [1], representing 50% of the theoretical value of methane.
japonica wastes at different temperatures (20–80 °C) with Among brown macroalgae, Sargassum is a potential source
HCl and industrial flue gas condensate did not improve sig- to produce biomethane by AD. It is an ideal biomass because
nificantly the biomethane yield [133]. of its high polysaccharides and negligible lignin content;

Table 2  Advantages and disadvantages of pretreatment methods [94]


Pretreatment method Advantages Disadvantages

Mechanical • Reduced cellulose crystallinity • High energy consumption


Biological • Lignin and hemicellulose degradation • Low hydrolysis rate
• Low energy requirement • Long reaction times
• Environmentally friendly
Dilute acid • Short reaction times (1–30 min) • High temperatures (160–220 °C) and pressures
• Removal of hemicellulose via hydrolysis to xylose • Formation of fermentation inhibitors
• Alters lignin structure
Hot water • Short reaction times (1–30 min) • High temperatures (160–220 °C)
• No chemical required • Formation of fermentation inhibitors
• Removal of hemicellulose
Alkali • Mild temperatures (25–160 °C) • Long reaction times (60 min—weeks)
• Removal of lignin and hemicellulose • Salt formation
• No formation of fermentation inhibitors • Chemical consumption (no recovery)
Ionic Liquids • Dissolution of cellulose and/or lignin • Expensive solvents
• Solvents are non-volatile • Solvents may be inhibitory to fermentation
Steam explosion • Short reaction times (1–15 min) • High temperatures (180–290 °C)
• Removal of hemicellulose and lignin • Formation of fermentation inhibitors
AFEX • Short reaction times (5–45 min) • No removal of hemicellulose or lignin
• Increased surface area • Not suitable for high lignin biomass
• Reduced cellulose crystallinity
• No formation of fermentation inhibitors

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2780 Waste and Biomass Valorization (2022) 13:2769–2793

therefore, it undergoes an almost complete hydrolysis. Nev- pelagic Sargassum and food wastes increased methane pro-
ertheless, the low C/N ratio (less than 20:1) and the presence duction when compared with mono-digestion of macroal-
of structurally complex polysaccharides, salts, sulfur poly- gae, because the addition of food waste optimizes the C/N
saccharides, and polyphenols could limit methane yields [6, balance, increased the concentration of macronutrients and
149]. Sargassum is potentially the largest natural source of provided lipids to the seaweed feed [98]. Other macroal-
polyphenols in the open ocean, reaching a content of 29.5 mg gae were co-digested with cattle manure [140], dairy slurry
­g−1 dw (dry weight) [50], but it can inhibit AD. Recently, [141, 159], sewage sludge, sugar industry wastewater [160],
methane yields from pelagic Sargassum were between 65 waste-activated sludge, wheat straw [139] both in batch and
and 145 L­ CH4 ­kgVS−1, corresponding to the 17–39% of the continuous processes [96].
theoretical yield [50]. In another study, three species of S. Finally, Sargassum could be used as a feedstock in a
natans and S. fluitans produced 113 L ­ CH4 ­kgVS−1. The low biorefinery with biogas recovery, to valorize all the compo-
methane potential of pelagic Sargassum can be attributed nents of macroalgae.
to its rich total indigestible fibre content (even higher than
30%, as shown in Table 1) [50]. Also the low lipid content
negatively affect the biogas production. Bioaccumulation of Heavy Metals
Since samples cannot be transported wet from the place in Sargassum and its Implications
of collection to the appropriate laboratories, they need to on Anaerobic Digestion
be dried out. However, the difference in BMP between wet
and dried Sargassum is not very significant [50]. Also the The proclivity of Sargassum to sequester heavy metals is a
difference in methane yields between washed and unwashed result of the high metal ion binding capacity of its cell wall
samples was not statistically significant [150]. Nevertheless, [161]. The presence of alginate and carboxylic groups in the
these data may vary since the composition of Sargassum Sargassum cell structure allow the capture of metal ions in
depends on the species, season, and location. Some authors water, in a greater or lesser capacity, depending on the pH
suggest that Sargassum mono-digestion is not sustainable of the seawater [20]. The binding mechanisms include ion
for energy extraction given its low bioconversion efficiency exchange, chelation, adsorption and ion entrapment in the
and unpredictable flow volume [6]. However, the potential polysaccharide network of the algae [74].
of Sargassum for biogas production could be fully exploited Toxic heavy metals detected in Sargassum include arse-
by appropriate pretreatments before AD (see Table 4), to nic, cadmium, copper, cobalt, chromium, iron, molybdenum,
increase the bioavailability of not easily fermentable poly- nickel, manganese, lead and zinc [73]. In a spatial and tem-
saccharides for microbial hydrolysis. poral study of Sargassum in the Mexican Caribbean only
Autoclaving provided the highest methane yield at 541 arsenic (24–172 ppm dry weight) and manganese (median
­LCH4 ­kgVS−1 from Sargassum sp. [157]. A fungal pretreat- 40–139 ppm dry weight) were present in all samples [74].
ment by Trametes hirsuta produced a 20% increase in A cause of concern is that 86% of samples presented arsenic
methane yields of Mexican Caribbean macroalgae [101]. concentrations above 40 ppm, the maximum allowable con-
Hydrothermal pretreatment of pelagic Sargassum prior to tent for seaweeds to be used as animal food under European
AD improved the methane yield and decreased the H ­ 2S regulations [162]. Arsenic concentration in organic matrices
concentration in biogas [75, 98]. Ensilage may address the destined for soil amendments, should not exceed the high-
problem of discontinuity, since it did not affect the methane est natural levels found in soil (1–40 ppm) [163]. Mexico
yield [154]. restricts the maximum allowable arsenic concentration in
In addition to pretreatments, a possible solution to low products for agricultural soils to 22 ppm [74].
methane yields could be co-digestion of Sargassum with It is likely that Sargassum acquires heavy metals in the
readily biodegradable substrates [98]. Co-digestion helps ocean, before entering coastal waters. Fernandez et al. [164]
increase C/N ratio, dilute salinity and inhibitors, balance identified sewage discharge, fertilizer and pesticide use as
nutrient supply, and overcome problems of Sargassum sea- main sources of contamination. More recently, Wang et al.
sonality by continuous biogas production. The co-digestion [5] indicated that increased deforestation and fertilizer use
of glycerol and S. muticum increased C/N ratio closer to in Brazil may be important sources of nutrients for the Great
the optimal value for AD and improved methane yield from Atlantic Sargassum Belt that extends from West Africa to
70 L ­kgVS−1 (only S. muticum) to 210 L ­kgVS−1 (50% glyc- the Gulf of Mexico. In this case, Sargassum is a promising
erol and 50% S. muticum) [158]. Co-digestion of Sargas- biomass for biosorption and bioremediation purposes.
sum sp. with glycerol and waste frying oil increased the bio- However, metal ions bound to a Sargassum -based
chemical methane potential by 56% and 46%, respectively, organic feedstock may lead to salt accumulation and reduced
compared to digestion of macroalga [156]. Co-digestion of anaerobic digestion performance [92]. Even cations like

13
Waste and Biomass Valorization (2022) 13:2769–2793 2781

magnesium, calcium and potassium can poison microbial digestion and strongly decreased the biogas production
cultures or foul an AD reactor [83]. In addition to lower [179], as well as Ag and ­CeO2 [180].
methane yields, the heavy metals in the digestate pose dis- Despite several works about nanoparticles-aided anaero-
posal problems and hinder any use as fertilizer [165]. Across bic digestion from different substrates, very few studied con-
several studies, arsenic is the most abundant and problematic cerned the macroalgal biomass and focused on the positive
toxic metal in Sargassum, with concentrations as high as effect of nanoparticles on the anaerobic digestion of green
231 ppm [166]. The downstream bioaccumulation issue of algae. The biogas production from green algae Enteromor-
arsenic and other heavy metals in digestate biomass and soils pha was increased by Ni, Co, ­Fe3O4, MgO nanoparticles
have prompted proposals for bioremediation. For instance, [181, 182], also in combination with a microwave pretreat-
arsenic content may be reduced in digestate after anaerobic ment [146, 183–185]. The best performances were obtained
digestion if Sargassum is mixed with other biomass sources after 170 h by adding 10 mg L ­ −1 of F
­ e3O4 or 1 mg L ­ −1 of
(e.g., wood chips) prior to AD [150]. Also, washing and Ni nanoparticles, resulting in cumulative biogas increase of
drying a Sargassum-based matrix prior to pretreatment and 28% and 26%, respectively. The biogas production from 20 g
AD, may reduce heavy metal content [142]. Biochar, a by- of dry algae powder was 624 mL for ­Fe3O4 and 618 mL
product of biomass pyrolysis, can be useful for AD [167], as for Ni [181]. Nevertheless, to the best of our knowledge,
it can act as an adsorbent of heavy metals and other diges- brown macroalgae has never been investigated concerning
tion inhibitors from the Sargassum-based feedstock [168]. this aspect. Moreover, the ecotoxicity of the nanoparticles-
Finally, the heavy metal contaminants can be removed from containing digestate and its suitable disposal need to be
seaweed by mobilization into a liquid phase and subsequent exploited. This point needs to be explored in the future to
metal ions adsorption [169]. ascertain the economic feasibility of improved methane
These bioremediation approaches for AD and digestate generation.
by-product are highly dependent on the nature and quan-
tity of the organic waste, process design and the material
balances of the heavy metals to avoid any waste treatment Conclusion: Perspectives, Challenges,
problems. and Next Steps

Efforts to cultivate algal biomass (e.g., microalgae) on a


Outlook: Nanoparticles large scale for energy purposes have proven costly, in part
due to high infrastructure costs for growing and harvest-
Nanotechnology has promising applications in enhancing ing [186]. On the other hand, the problematic inundation
the methane concentration and biogas production. Indeed, of pelagic Sargassum biomass (i.e., macroalgae) on coast-
nanoparticles can improve the activity of organic matter- lines presents a “free” and ready-to-use marine crop as a
degrading microorganisms in an anaerobic digester by potential source for products in major commercial sectors
biostimulating the bacterial cells [170]. Typically, possible in food, agriculture, construction, chemicals, and biofuels
good nanoparticles are based on zero-valent metals, metal [187, 188].
and metallic oxides or carbon [171]. Faisal et al. summa- Indeed, beach or near-shore invasions of pelagic Sargas-
rized that adequate concentrations of several nano-additives sum in the Caribbean require strategies to minimize detri-
­(CeO2, ­Fe2O4, ­Fe2O3, ­Fe3O4, Fe/SiO2, Pt/SiO2, Co/SiO2, Ni/ mental effects and turn this problem into an opportunity.
SiO2, Co, Ni, Fe, ZnO) increased methane production [172]. Sargassum can have a higher energy potential compared to
­Fe3O4 nanoparticles are the most investigated materials other biomasses and its use in anaerobic digestion for pro-
thanks to their high biocompatibility and low toxicity. They duction of methane can reduce drying costs before process-
were implemented to enhance the biogas production from ing [186]. In addition, Sargassum has low lignocellulose
cattle dung slurry [173, 174], organic fraction of municipal content which favors production of methane [187]. There-
solid waste [175], poultry litter [176], heat pretreated waste fore, accumulated macroalgae is a renewable waste biomass
sludge [177]. Nevertheless, the selection of type, size and to be anaerobically digested to biomethane (and biohydrogen
concentration of nanoparticles is crucial and have a strong by dark fermentation). However, the readiness of Sargassum
impact on biogas yield, anaerobic digestion process stability, comes at a cost, as specialized machinery and boat harvest-
and ­H2S and other impurities in biogas production [178]. ers are needed to collect Sargassum from coastlines. Also,
Some nanoparticles could inhibit the biogas production rate, despite the constant influx of Sargassum in coasts since
by suppressing acetoclastic methanogens and inhibiting 2011, the seasonal availability for long-term and sustain-
­H2-consuming methanogenes [171]. As an example, ZnO, able use, remains a concern [98].
CuO, ­Mn2O3 and ­Al2O3 affected negatively the anaerobic The potential of algal biomass for bioenergy produc-
tion has been widely recognized, however few studies are

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Table 3  Biomethane production by AD of macroalgae in batch experiments


Macroalgae Temperature Time Pretreatment Methane yield References
(°C) (days) (LCH4 ­kgVS−1)

Ascophyllum nodosum Brown 38 14 Cutting, mechanical pretreatment 169 [118]


by a Hollander beater (15 min)
Brown algae 35 60 Grinding 179 [120]
Fucus serratus 35 109 Drying (room temperature), milling 161 (biogas) [121]
−1
37 21 None 64.2 ­(Lbiogas ­kgTS ) [122]
Mechanical by a Hollander beater 181.2 ­(Lbiogas ­kgTS−1)
Fucus vesiculosus 37 20 Washing, drying (53 °C), hydro- 37–71 [123]
thermal pretreatment (20–80 °C)
Washing, drying (53 °C), thermo- 37–65
acidic pretreatment (20–80 °C,
FGC)
Washing, drying (53 °C), thermo- 52–116
acidic pretreatment (20–80 °C,
HCl)
21 None 71.5 ­(Lbiogas ­kgTS−1) [122]
−1
Mechanical by a Hollander beater 230.5 ­(Lbiogas ­kgTS )
22 Freezing (− 18 °C), mechanical 68.4–84.3 [124]
pre-treatment
Freezing (− 18 °C), mechani- 78.9–130.1
cal pre-treatment, microwave
(1.5 min)
Freezing (− 18 °C), mechanical 116.6–146.9
pre-treatment, microwave (3 min)
25 Unwashed, chopping 120 [125]
Washing, chopping 134
52 None 67 [126]
Thermal pre-treatment (50 °C) 41
Mechanical pre-treatment (50 °C) 92
Enzymatic pre-treatment with cel- 49
lulase, hemicellulase, pectinase,
protease (50 °C)
Mechanical + enzymatic pre-treat- 131
ment (50 °C)
Fucus vesiculosus + Fucus serratus 37 20 Mechanical (washing, grinding) 140.5 [127]
Mechanical + Ultrasounds 235
Mechanical + Microwave 220
Mechanical + Ultrasounds + Micro- 260
wave
Laminaria digitata 20 54 Drying (75 °C), milling 111 [128]
35 Drying (75 °C), milling 184
21 Washing, cutting, oven drying 222.6 [129]
(105 °C), grinding, dark fermen-
tation
Washing, cutting, oven drying 282.2
(105 °C), grinding, hydrothermal
pretreatment, dark fermentation

13
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Table 3  (continued)
Macroalgae Temperature Time Pretreatment Methane yield References
(°C) (days) (LCH4 ­kgVS−1)

Washing, cutting, oven drying 271


(105 °C), grinding, enzymolysis,
dark fermentation
Washing, cutting, oven drying 294.2
(105 °C), grinding, hydrothermal
pretreatment, enzymolysis, dark
fermentation
Washing, cutting, oven drying 164.9
(105 °C), grinding, hydrother-
mal dilute acid pretreatment
(HTDAP), dark fermentation
Washing, cutting, oven drying 159.4
(105 °C), grinding, hydrother-
mal dilute acid pretreatment
(HTDAP), enzymolysis, dark
fermentation
32 None 228 (biogas) [130]
Enzymatic pretreatment 72–232 (biogas)
Organic acid pretreatment 69–237 (biogas)
Combined enzymatic + acid pre- 76–243 (biogas)
treatment
35 No washing, oven drying (70 °C), 235.4 [93]
milling
No washing, freezing (− 20 °C), 191.7
oven drying (70 °C), milling
No washing, shock-freezing with 239.7
liquid nitrogen, freeze-drying,
milling
Washing, oven drying (70 °C), 202.9
milling
Washing, freezing (− 20 °C), oven 248.1
drying (70 °C), milling
Washing, shock-freezing with 257.7
liquid nitrogen, freeze-drying,
milling
109 Drying (room temperature), milling 246 [121]
37 21 None 103.3 ­(Lbiogas ­kgTS−1) [122]
Mechanical by a Hollander beater 156.4 ­(Lbiogas ­kgTS−1)
30 None 280 [131]
Washing with cold water (15 °C), 303
cutting
Washing with cold water (15 °C), 326
maceration
Washing with hot water (40 °C), 307
cutting
Washing with hot water (40 °C), 308
maceration
45 54 Drying (75 °C), milling 141 [128]
−1
Laminaria hyperborea 35 N.A Chopping, blending 65.6 (L ­kgTS ) [132]
Laminaria japonica 35 75 Washing, drying (60 °C), milling 267.5 [115]
N.A 22 Untreated 172 [133]

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Table 3  (continued)
Macroalgae Temperature Time Pretreatment Methane yield References
(°C) (days) (LCH4 ­kgVS−1)

Thermochemical pretreatment with 156–171


0.05–0.5 M HCl (20 °C)
Thermochemical pretreatment with 150–180
0.05–0.5 M HCl (50 °C)
Thermochemical pretreatment with 149–168
0.05–0.5 M HCl (80 °C)
Laminaria sp. (L. digitata, Saccha- 38 14 Cutting, beating (15 min) 240 [118]
rina latissima, L. hyperborea)
25 Cutting 328 [87]
Cutting, beating (10 min) 335
Cutting, drying (24 h), ball milling 241–260
Cutting, microwave 244
Laminaria spp. 50 21 Mechanical by a Hollander beater 430 (L ­kgTS−1) [134]
Macroalgae consortium 38 29 Washing 81 [101]
Washing, biological pretreatment 104
(Bm-2 strain white rot fungi)
Washing, biological pretreatment 86
(enzymatic broth)
Nizimuddinia zanardini 37 40 Washing, drying (40 °C), milling 117 [135]
Washing, drying (40 °C), milling, 143
hot water pretreatment
Pelvetia caniculata 37 21 None 159.3 ­(Lbiogas ­kgTS−1) [122]
Mechanical by a Hollander beater 444.3 ­(Lbiogas ­kgTS−1)
340 [136]
Saccharina latissima 35 11 Washing, drying (105 °C), pulveri- 281.4 [137]
zation, dark fermentation
Washing, drying (105 °C), pulveri- 318.8
zation, hydrotermal pretreatment
(100 °C), dark fermentation
Washing, drying (105 °C), pulveri- 344.6
zation, hydrotermal pretreatment
(120 °C), dark fermentation
Washing, drying (105 °C), pulveri- 345.1
zation, hydrotermal pretreatment
(140 °C), dark fermentation
Washing, drying (105 °C), pulveri- 337.8
zation, hydrotermal pretreatment
(160 °C), dark fermentation
Washing, drying (105 °C), pulveri- 278.7
zation, hydrotermal pretreatment
(180 °C), dark fermentation
109 Drying (room temperature), milling 335 [121]
60 Drying (40 °C), chopping 209 [138]
37 119 Grinding 223 [139]
Grinding, pretreatment (130 °C, 268
10 min)
Grinding, pretreatment (160 °C, 260
10 min)
53 34 Washing, chopping 340 [140]

13
Waste and Biomass Valorization (2022) 13:2769–2793 2785

Table 3  (continued)
Macroalgae Temperature Time Pretreatment Methane yield References
(°C) (days) (LCH4 ­kgVS−1)

Saccorhiza polyschides 35 109 Drying (room temperature), milling 255 [121]


Chaetomorpha linum Green 53 34 Washing, chopping 166 [140]
Green algae 35 60 Grinding 256 [120]
Ulva spp. 35 109 Drying (room temperature), milling 191 [121]
Ulva lactuca 35 30 Untreated 183.2 [141]
Wiltered, unwashed 165
Washing, drying 250.2
Wiltered, washing 221.1
37 58 Chopping 162 [142]
37 65 Washing, sun-drying, oven-drying 498.75 [143]
(50 °C), milling, ozonation pre-
treatment (30 min)
53 34 Washing, chopping 152 [140]
55 42 Chopping 174 [142]
55 42 Maceration 271 [142]
Washing, chopping 171
Washing, maceration 200
Washing, pretreatment (110 °C, 157
20 min)
Washing, pretreatment (130 °C, 187
20 min)
Drying (45 °C), grinding 176
Chaetomorpha linum + Gracilari- Green/Red 25 57 None 50 [144]
opsis longissima
35 160
55 < 10
Filamentous red algae Red 37 52 None 212 [126]
Thermal pre-treatment (50 °C) 139
Mechanical pre-treatment (50 °C) 223
Enzymatic pre-treatment with cel- 167
lulase, hemicellulase, pectinase,
protease (50 °C)
Mechanical + enzymatic pre-treat- 217
ment (50 °C)
Gracilaria gracilis 37 21 None 81.8 ­(Lbiogas ­kgTS−1) [122]
−1
Mechanical by a Hollander beater 171.8 ­(Lbiogas ­kgTS )
Gracilaria vermiculophylla 53 34 Washing, chopping 132 [140]
Palmaria palmata 35 N.A None 308 [145]
Maceration (20 °C) 328
Thermal pretreatment (120 °C) 296
Thermal pretreatment (160 °C) 269
Thermal pretreatment (180 °C) 268
Thermal pretreatment (200 °C) 211
NaOH + Thermal pretreatment 282
(160 °C)
KCl + Thermal pretreatment 268
(160 °C)
60 Drying, chopping + NaOH 363.5 [145]
Drying (40 °C), chopping 257 [138]

13
2786 Waste and Biomass Valorization (2022) 13:2769–2793

available on the economic feasibility of their exploitation. carbon biomass (e.g., food waste, woodchips, paper, saw-
The biochemical methane potential (BMP) of Sargassum dust) can optimize methane yields as much as five times
ranges from 41.8 to 541 L/kgVS, strongly dependent on sea- [98, 187]. As an example, energy and economic analyses
sonality, sampling timing, pretreatments, and operating con- were recently implemented also for the Caribbean islands
ditions. Sargassum accumulation in the Caribbean Sea and of St. Lucia and Grenada, where dried Sargassum beached
Central Atlantic Ocean is estimated at 47.2 million metric for around 2 months did not resulted very productive for
tons for 2020 and the digestion of this biomass would poten- anaerobic digestion, except in co-digestion with food waste
tially yield 94,600 GWh/yr. Notwithstanding the energy [67]. Moreover, a very recent publication assessed the
potential and biomass readiness of Sargassum, its mono- techno-economic feasibility and environmental impact of
digestion for methane production resulted in low yields well pelagic Sargassum exploitation in Barbados [189]. Here, the
below the theoretical maximum [186], that impeded the sus- co-digestion of Sargassum and raw food wastes at a mass
tainable large scale exploitation as feedstock [98]. ratio of 25:75 resulted economically sustainable, produc-
This review has extensively covered mitigating actions ing—from 15,750 tons of substrate per year—0.69 GWh of
to improve methane production from Sargassum. Adequate electricity, 1.04 GWh of heat and 15,750 tons of digestate,
pretreatments to break down the cell wall, and co-digestion for a total potential income of US $ 12.76 million.
with other biomass sources may enhance the biogas yield In addition, the selection of suitable nanoparticles may
and make the process more cost-effective. Specifically, co- yield greater biogas production and needs attention. Finally,
digestion aimed at increasing the carbon to nitrogen ratio we consider reasonable the operation of biomethanation
(C:N) of Sargassum from 10 to 30, as the addition of high in local small and medium sized biogas plants to produce

Table 4  Biomethane production by AD of Sargassum species in batch experiments


Macroalgae Temperature Time Pretreatment Methane yield References
(°C) (days) [LCH4 ­kgVS−1]

Macroalgae consortium 38 29 Washing 81 [101]


Washing, biological pretreatment 104
S. natans I N.A 28 None 65.8 [50]
S. natans VIII 145.1
S. fluitans 112.7
Mixed pelagic Sargas- 35 21 Untreated 48.23 [98]
sum (S. fluitans, S.
natans)
Hydrothermal 102.52
Washing, sun-drying (2 weeks), heating (80 °C) 41.8 [75]
Washing, sun-drying (2 weeks), heating (80 °C), hydrothermal 116.7
pretreatment
S. muticum N.A 30 Drying (105 °C, grinding) 166–208 [151]
30 40 Washing, grinding 102 [152]
Washing, grinding, extraction, autohydrolysis (150 °C) 170
35 40 Grinding 130 [153]
37 28 Unwashed 225 [150]
Washing 177
Untreated 100 [154]
Untreated, ensilage (60 days) 110
Chopping, ensilage (60 days) 60
36 Grinding, unwashed 128.2–139.7 [155]
Grinding, washing 163.2–170.2
Sargassum sp. 35 60 Washing, air-drying, milling 77.7–327.5* [81]
−1
37 42 Drying (37 °C), milling 181 L ­kgCOD [156]
Drying (room temperature), milling, autoclaving, dark fermenta- 541 [157]
tion

*Increasing methane yield with decreasing sodium concentration from 24.08 to 0.49 g/L

13
Waste and Biomass Valorization (2022) 13:2769–2793 2787

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