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Microalgae in Health
and Disease Prevention
Edited by
Ira A. Levine
Natural and Applied Sciences
University of Southern Maine
Lewiston, ME
United States
Joël Fleurence
University of Nantes
Nantes
France
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Notices
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products, instructions, or ideas contained in the material herein.
ISBN: 978-0-12-811405-6
Cover Courtesy: Courtesy of Petr Znachor, Institute of Hydrobiology, Biology Centre CAS.
To Doctor, Director, and Manager Levines
for all the nachas you bring me. To Laurie, my guiding light
and best friend and to baby Ari Makai, the 8th generation
of an only son of an only son, keep our name with pride and integrity.
You all fill my life with hope and love.
Contents
vii
viiiContents
List of Contributors
Zouher Amzil IFREMER, Nantes, France Matthew L. Julius St. Cloud State University, St. Cloud,
Jean-Marie Bard Faculté des Sciences Pharmaceutiques MN, United States
et Biologiques, EA2160 – Mer Molécules Santé Jang K. Kim Incheon National University, Incheon,
(MMS) – IUML (Institut Universitaire Mer et Littoral) – Republic of Korea
FR 3473 CNRS – Centre de Recherche en Nutrition Ira A. Levine University of Southern Maine, Lewiston,
Humaine Ouest, Nantes, France; Institut de Cancérologie ME, United States
de l’Ouest, Centre René Gauducheau, Saint-Herblain,
France Michael W. Lomas National Center for Marine Algae and
Microbiota (NCMA), East Boothbay, ME, United States
Michael A. Borowitzka Murdoch University, Murdoch,
WA, Australia; OzAlgae, Cygnet, TAS, Australia Virginie Mimouni University of Le Mans, Le Mans-Laval,
France
Nathalie Bourgougnon Université Bretagne Sud, Vannes,
France Michèle Morançais Université de Nantes, Nantes Cedex 3,
France
Intan C. Dewi Le Mans Université, Le Mans, France
Jean-Luc Mouget Le Mans Université, Le Mans, France
Amandine M.N. Caruana IFREMER, Nantes, France
Hassan Nazih Faculté des Sciences Pharmaceutiques et
Yusuf Chisti Massey University, Palmerston North, Biologiques, EA2160 – Mer Molécules Santé (MMS) –
New Zealand IUML (Institut Universitaire Mer et Littoral) – FR 3473
Laurence Coiffard University of Nantes, Nantes, France CNRS – Centre de Recherche en Nutrition Humaine
Céline Couteau University of Nantes, Nantes, France Ouest, Nantes, France
Aurélie Couzinet-Mossion University of Nantes, Nantes, Jihae Park Ghent University Global Campus, Incheon,
France Republic of Korea
Justine Dumay Université de Nantes, Nantes Cedex 3, P.D. Rajakumar Imperial College London, Kensington,
France United Kingdom
Charlotte Falaise Le Mans Université, Le Mans, France Julianne P. Sexton National Center for Marine Algae and
Microbiota (NCMA), East Boothbay, ME, United States
Joël Fleurence University of Nantes, Nantes, France
Lionel Ulmann University of Le Mans, Le Mans-Laval,
Joe M. Fox Texas A&M University-Corpus Christi, Corpus France
Christi, TX, United States; Texas A&M AgriLife
Research, Corpus Christi, TX, United States Gaëtane Wielgosz-Collin University of Nantes, Nantes,
France
Taejun Han Ghent University Global Campus, Incheon,
Republic of Korea; Incheon National University, Charles Yarish University of Connecticut, Stamford, CT,
Incheon, Republic of Korea United States
Claire Hellio Universitaire Européen de la Mer (IUEM) - Paul V. Zimba Texas A&M University-Corpus Christi,
UBO – UEB Technopôle Brest-Iroise, Plouzané, France Corpus Christi, TX, United States
xi
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About the Editors
Dr. Ira A. Levine, Ph.D. is a tenured Professor of natural and applied sciences at the
University of Southern Maine, President and Board Chair of the Algae Foundation,
Executive Director of Professors Beyond Borders, and the CEO of Algal Aquaculture
Professionals, LLC. Dr. Levine was: selected as the Trustee Professor of University
of Southern Maine for 2017–18. He was awarded the U.S. State Department’s distin-
guished Fulbright New Century Scholar in 2009–10 and Chair Fulbright in 2016–17.
He was a visiting Professor of biology at Duke University in 2007–08. Dr. Levine com-
bines 33 years of basic and applied research in physiological ecology and cultivation
of algae, algal farm management, and aquaculture engineering. His farming experience
includes open-ocean and pond cultivation in Canada, China, Indonesia, Japan, Malaysia,
Philippines, and USA (Hawaii, Florida, and Maine). Current efforts include algal cultivar
enhancement for biofeeds, human nutraceuticals, and cosmeceuticals, fine chemicals, and
algal-based biofuels.
Dr. Joël Fleurence, Ph.D., is a Professor of Marine Biology and Biochemistry at the
University of Nantes. He is one of the two Directors of the Research Laboratory “Sea,
Molecules, Health.” He is a member of the University National Council since 2007 and
was elected President of the section “Biology of organisms” since 2017. He is a senior
scientist and an international expert on the seaweed valorization (120 international pub-
lications including patents). In 1985, he began his research career in the pharmaceuti-
cal industry in the French Company Roussel Uclaf. In 1990, he was recruited by the
Institute of Valorization of Seaweeds (CEVA, Brittany, France) to lead researches about
the chemical composition and nutritional properties of macroalgae. Professor Fleurence
has participated in the establishment of the French regulation on marine algae used as sea
vegetables. In 1994, he arrives as a head of laboratory “Proteins and Quality” at IFREMER
(Research French Organism for the Sea Exploitation) and develops research on the nutri-
tional properties of seaweed protein for use in human or animal food. Since 2002, he is a
Professor at the University of Nantes and leads research on the development of seaweed
uses as protein or pigment sources for the industry.
xiii
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Chapter 1
Chapter Outline
References8
“Vilor Alga” (translated as more vile or worthless than algae) wrote Virgil, the Latin poet, in 30 BCE. Civilizations were aware
of the role of algae in human health long before Virgil. The use of microalgae dates back 1000 years in Asia and 700 years by
the Aztecs, approximately 3700 years after the first documented use of seaweeds. Contrary to the use of microalgae as a func-
tional food or health tonic, there are historical indications of algal-based pathogens, including: The first plaque visited upon
the Pharaoh of Egypt in the Bible’s book of Exodus, which could be considered a reference to a red tide; the Caribbean in the
1500’s (Halstead, 1978); and the South Pacific in 1606 by the Spanish explorer de Quinos (Mills and Passmore, 1988) with
symptoms brought on by ingestion of shell or finfish, direct skin contact, and/or respiratory inhalation.
Microalgae (phytoplankton) are a diverse assemblage of plantlike, predominantly aquatic, unicellular, multicellular,
or colonial forms; photosynthetic; chlorophyll “a” containing organisms found in the atmosphere, on mountain tops, and
200–300 m below the ocean-air interface. The microalgae are evolutionarily diverse occupying two domains, Eukaryota and
Bacteria, and include, but not limited to the, cyanobacteria (blue-green algae), Charophyta (chara), Chlorophyta (green),
Rhodophyta (red), Ochrophyta (brown), Glaucophyta, Euglenophyta, Cryptophyta, Chrysophyta, Bacillariophyceae (dia-
toms), and Dinophyceae (dinoflagellates). The approximately 41,000 described microalgal species are segregated by photo-
synthetic pigment content, carbohydrate food reserve, cell wall components, and flagella construction and orientation. This
eclectic group has evolved over the last 2500 million years (1600–1900 million years older than the seaweeds), occupying
a variety of ecological niches, that is, planktonic, benthic (growing in sand, mud, soil), epilithic, epiphytic (growing on
other algae, seagrasses, and trees), symbiotic relationships with fungi and invertebrates, atmospheric, and in rare occa-
sions, parasitic. There are additional groups of algae, which can form biofilms, colonial formations, mats, and turfs. The
term “microalgae” will include both the eukaryotic and cyanobacterial forms for the sake of discussion in this chapter.
Despite the total number of described microalgae, perhaps only a few hundred species have been investigated thoroughly,
only several dozens of which are fully understood, with their nutritional, health, pathogenic, or commercial potential truly
delineated. There is much work to be done with this eclectic group before we can fully appreciate the value of microalgae
in health and disease prevention. The algae play an essential role as the foundation of all aquatic food webs and in the
production of more than half of our globe’s oxygen. Additionally, via photosynthesis and nitrogen fixation, microalgae act
as major components of the carbon (Falkowski and Raven, 2007) and nitrogen cycles (Fowler et al., 2013), respectively.
As algae in general and microalgae in particular have played an ever increasing role in humans’ diet, health, and well-
being, their utilization and product development have rapidly expanded our appreciation for the diverse phytochemicals
that the algae produce (Table 1.1). Humans augment traditional medical practices by incorporating nutraceuticals and
supplements, thus acknowledging the relationship between health and diet. Microalgae have been a significant component
of mainstream dietary supplements for the past generation. The most common commercially exploited microalgal genera
are Arthrospira (Spirulina), Chlorella, Dunaliella, and Haematococcus. Benefits include: immune system enhancement,
reduction in viral infections and cancer onset, pre- and probiotic effects, increase in hemoglobin concentrations, and the
reduction in blood sugar levels and bacterial populations. Historically, Chlorella and “plankton soup” were utilized as far
back as 1942, to aid leprosy patients by supporting increase in weight, energy, and general health (Barrow and Shahidi,
2008). Additionally, microalgal-sourced, omega 3 and 6 long chain polyunsaturated fatty acids (PUFA’s) are utilized for
Antioxidant
Carotenoids Phenolic Acids Stilbenese Vitamins Phycobiliproteins Sterols Stanols Polysaccharides
α-carotene Gallic Resveratrol Provitamin A C-phycocyanin Cholesterol Cholestanol Sulfated
polysaccharides
β-carotene Chlorogenic Vitamin E Allophycocyanin β-sitosterol Stigmastanol Spirulans
Lutein Vanillic Folic acid Phycoerythrin Campesterol β-glucans
Zeaxanthin Syringic Ascorbic acid 24-Methyldiene
cholesterol
Astaxanthin ρ-coumaric Cobalamin Fucosterol
Liu, R., 2004. Potential synergy of phytochemicals in cancer prevention: mechanism of action. Journal of Nutrition 134, 3479–3489; Prakash, D., Gupta, C., Sharma, G., 2012. Importance of phytochemicals
in nutraceuticals. Journal of Chinese Medicine Research and Development 1 (3), 70–78 as adopted from Raposo, M., de Morais, A., 2015. Microalgae for the prevention of cardiovascular disease and stroke.
Life Sciences 125, 32–41.
Algae: A Way of Life and Health Chapter | 1 3
neurological and cardiac development, and support decrease in skin diseases, rheumatism, coronary heart disease, hyper-
tension, cancer, and cholesterol levels (Mata et al., 2010). Haematococcus pluvialis produces the pigment astaxanthin,
which is recently approved as a dietary supplement and is the feed additive responsible for the reddish pink flesh of aqua-
cultured salmon. Astaxanthin ingestion has been linked to antibody production; antitumor and anti-inflammatory activity;
inhibition of colon, bladder, liver, mammary, and oral cancers; decreasing risk of Parkinson’s and Alzheimer’s diseases; and
improvement in cardiovascular health (Mata et al., 2010).
Through adaptive evolution and metabolic diversity, microalgae have developed a variety of bioactive compounds.
While many of these compounds have biomedical properties that benefit human health, few act as neurological and gastro-
intestinal toxins. Curiously, freshwater microalgal-based toxins are produced primarily by cyanobacteria, whereas marine
microalgal-based toxins are produced by dinoflagellates and diatoms. The toxins tend to be heat-stable, tasteless, odorless,
resistant to acids, and cooking has no effect on them (Backer et al., 2004). Table 1.2 includes the toxins, source algae, route
of acquisition, and clinical manifestation.
The use of microalgae, especially Chlorella and Arthrospira, as dietary supplements must be tempered due to potential
contamination from cultivation, harvesting, processing, and/or storage stages of supplement preparation. Contaminations
can include pathogenic alternative species, heavy metals, cyanotoxins, and inorganic arsenic. Quality control and quality
assurance best practices are needed to reduce or eliminate potential contamination sources, and the purchase of supplements
should be restricted to highly qualified and certified producers, packagers, and distribution concerns (Rzymski et al., 2015).
With the continued use and development of algal-based supplements, additional clinical studies and precautions should
be undertaken in the best interest of the public. Rzymski et al. (2015) list a few best practices to follow:
1. It is not advisable to use Chlorella and Spirulina-based products simultaneously.
2. Use of commercial microalgae-based products should be avoided in individuals suffering from renal failure and suscep-
tible to Al compounds due to potentially high level of Al contamination in these supplements.
3. Use of microalgae-based products should be avoided in individuals suffering from autoimmune diseases, as a relapse of
symptoms can occur.
4. Use of microalgae-based products of unknown origin should be avoided.
5. Use of microalgae-based products in infants and children should be limited.
6. All microalgal-based products should be subject to quality screening and safety assessments performed routinely by
independent agencies prior to registration.
7. All microalgae-based products characterized by detectable cyanotoxin content and significant levels of Al and other
toxic metals should be systematically eliminated from the market.
Drug discovery over the past 70 years has resulted in nearly 28,000 compounds isolated from marine organisms, only 7
of which have been approved for human pharmaceutical use. The drug approval pipeline has an additional 26 in phase I or
II trials. The candidates include 23 anticancer, 2 schizophrenia and Alzheimer’s, and 1 chronic pain treatments (Lauritano
et al., 2016). Most of the marine drug discoveries originated in sponges or ascidians which are difficult to culture and whose
standing stocks do not represent a commercial source of finished drug source material. The ease of collection, isolation,
identification, cultivation, harvesting, and extraction of microalgae and their metabolites represent an attractive alternative
research group. Algae’s evolution over the course of 2500 million years, its diversity, and ability to inhabit extreme environ-
ments have resulted in novel defense, communication, and survival techniques, adding to their human drug and nutraceuti-
cal potentiality (Lauritano et al., 2016). Numerous pharmacological activities have been reported and tested (Tables 1.3 and
1.4) such as: allelopathic, anti-inflammatory, anticancer, antiobese, antidiabetic, antiangiogenic, antimalarial, antioxidant,
antibacterial, antiviral, and growth inhibiting properties (Gastineau et al., 2014; Guedes et al., 2013; Mimouni et al., 2012;
Nigjeh et al., 2013; Patterson et al., 1990a,b; Peng et al., 2011; Samarakoon et al., 2013). However, one note of caution
is that drug discovery in microalgae is a function of cultivation of environmental regimes resulting in metabolic plasticity
(Lauritano et al., 2016). Metabolite production and bioactivity levels vary as a function of habitat and seasonality. Primary
and secondary metabolites production and concentration are a function of: growth phase (Vidoudez and Pohner, 2012),
clones (Gerecht et al., 2011), light (Depauw et al., 2012), temperature (Huseby et al., 2013), culturing media (Alkhamis and
Qin, 2015), grazing pressure (Pohnert, 2002), extraction method (Juttner, 2001), and many other factors (Chen et al., 2011).
An example of metabolic plasticity is the elevated inhibition of biofilm formation by Leptocylindrus danicus and L. aporus,
and anticancer activity by Skeletonema marioni in nitrogen and phosphorus starved growth media.
The progress of phycology, the study of algae, within the public consciousness can be summarized by a seminar given by
the author at Middlebury College, Middlebury, Vermont, USA in March 2010, “The Road from Science Geek to Being Cool,
Algal Physiological Ecology: a Global Economic Development Engine.” As algae and algal-based biofuels became a research
and development priority in the United States during the 21st century, the once obscure field is now experiencing a surge of
4
TABLE 1.2 Microalgal Toxins (Manganelli, 2016; Backer et al., 2004; Morris, 1999)
Planktothrix Neurotoxin
Anabaena
Nostoc
Synechocystis
Cyanobium
Arthrospira
Limnothrix
Phormidium
Hapalosiphon
Umezakia
Aphanizomenon
Raphidiopsis
Anabaena
Aphanizomenon
Cylindrospermum
Microcystis
Planktothrix
Raphidiopsis
Raphidiopsis
Anabaena
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Under the act of July 17, 1862.
August 4, 1862—The President ordered a draft of three hundred
thousand militia, for nine months unless sooner discharged; and
directed that if any State shall not, by the 15th of August, furnish its
quota of the additional 300,000 authorized by law, the deficiency of
volunteers in that State will also be made up by special draft from the
militia. Wednesday, September 3, was subsequently fixed for the
draft.
May 8, 1863—Proclamation issued, defining the relations of aliens
to the conscription act, holding all aliens who have declared on oath
their intention to become citizens and may be in the country within
sixty-five days from date, and all who have declared their intention to
become citizens and have voted.
June 15, 1863—One hundred thousand men, for six months, called
to repel the invasion of Maryland, West Virginia, Ohio, and
Pennsylvania.
October 17, 1863—A proclamation was issued for 300,000
volunteers, to serve for three years or the war, not, however,
exceeding three years, to fill the places of those whose terms expire
“during the coming year,” these being in addition to the men raised
by the present draft. In States in default under this call, January 5,
1864, a draft shall be made on that day.
February 1, 1864—Draft for 500,000 men for three years or during
the war, ordered for March 10, 1864.
March 14, 1864—Draft for 200,000 additional for the army, navy
and marine corps, ordered for April 15, 1864, to supply the force
required for the navy and to provide an adequate reserve force for all
contingencies.
April 23, 1864—85,000 one hundred day men accepted, tendered
by the Governors of Ohio, Indiana, Illinois, Iowa, and Wisconsin;
30,000, 20,000, 20,000, 10,000 and 5,000 being tendered
respectively.
Sec. 8. That all persons in the naval service of the United States,
who have entered said service during the present rebellion, who have
not been credited to the quota of any town, district, ward, or State, by
reason of their being in said service and not enrolled prior to
February twenty-four, eighteen hundred and sixty-four, shall be
enrolled and credited to the quotas of the town, ward, district, or
State, in which they respectively reside, upon satisfactory proof of
their residence made to the Secretary of War.
GUERRILLAS.
After the President had issued his first call, Douglas saw the
danger to which the Capitol was exposed, and he promptly called
upon Lincoln to express his full approval of the call. Knowing his
political value and that of his following Lincoln asked him to dictate
a despatch to the Associated Press, which he did in these words, the
original being left in the possession of Hon. George Ashmun of
Massachusetts:
“April 18, 1861, Senator Douglas, called on the President, and had
an interesting conversation, on the present condition of the country.
The substance of it was, on the part of Mr. Douglas, that while he was
unalterably opposed to the administration in all its political issues,
he was prepared to fully sustain the President, in the exercise of all
his Constitutional functions, to preserve the Union, maintain the
Government, and defend the Federal Capitol. A firm policy and
prompt action was necessary. The Capitol was in danger, and must
be defended at all hazards, and at any expense of men and money.
He spoke of the present and future, without any reference to the
past.”
Douglas followed this with a great speech at Chicago, in which he
uttered a sentence that was soon quoted on nearly every Northern
tongue. It was simply this, “that there now could be but two parties,
patriots and traitors.” It needed nothing more to rally the Douglas
Democrats by the side of the Administration, and in the general
feeling of patriotism awakened not only this class of Democrats, but
many Northern supporters of Breckinridge also enlisted in the Union
armies. The leaders who stood aloof and gave their sympathies to the
South, were stigmatized as “Copperheads,” and these where they
were so impudent as to give expression to their hostility, were as
odious to the mass of Northerners as the Unionists of Tennessee and
North Carolina were to the Secessionists—with this difference—that
the latter were compelled to seek refuge in their mountains, while the
Northern leader who sought to give “aid and comfort to the enemy”
was either placed under arrest by the government or proscribed
politically by his neighbors. Civil war is ever thus. Let us now pass to
The first session of the 37th Congress began July 4, 1861, and
closed Aug. 6. The second began December 2, 1861, and closed July
17, 1862. The third began December 1, 1862 and closed March 4,
1863.
All of these sessions of Congress were really embarrassed by the
number of volunteers offering from the North, and sufficiently rapid
provision could not be made for them. And as illustrative of how
political lines had been broken, it need only be remarked that
Benjamin F. Butler, the leader of the Northern wing of Breckinridge’s
supporters, was commissioned as the first commander of the forces
which Massachusetts sent to the field. New York, Pennsylvania, Ohio
—the great West—all the States, more than met all early
requirements. So rapid were enlistments that no song was as popular
as that beginning with the lines:
“We are coming, Father Abraham,
Six hundred thousand strong.”
The first session of the 37th Congress was a special one, called by
the President. McPherson, in his classification of the membership,
shows the changes in a body made historic, if such a thing can be, not
only by its membership present, but that which had gone or made
itself subject to expulsion by siding with the Confederacy. We quote
the list so concisely and correctly presented:
SENATORS.
REPRESENTATIVES.
MEMORANDUM OF CHANGES.
IN SENATE.
IN HOUSE OF REPRESENTATIVES