C H A P T E R

3
Serratia
Soma Barman1, Satya Sundar Bhattacharya1,
Narayan Chandra Mandal2
1
Soil and Agro-Bioengineering Laboratory, Department of Environmental Science, Tezpur
University, Tezpur, Assam, India; 2Mycology and Plant Pathology Laboratory, Department of
Botany, Visva-Bharati, Santiniketan, West Bengal, India

1. Introduction

Plants are colonized by a number of (micro) organisms that can reach cell densities greater
than the number of plant cells. To date, the interaction between plants and microbes has been
studied in depth for diverse symbiotic rhizobia and mycorrhizal fungi. The rhizosphere, that
is, the narrow region surrounding plant roots, is influenced by the activities of several micro-
organisms and is considered one of the most composite ecosystems on Earth (Pierret et al.,
2007; Jones and Hinsinger, 2008; Raaijmakers et al., 2009). A widespread research in the pre-
vious few decades has emphasized the role of both Gram-positive as well as Gram-negative
bacterial strains as promising biological control agents (Kumar et al., 2005; Ge et al., 2007;
HoÈfte and Altier, 2010; Selim et al., 2010). Rhizospheric bacteria can overall plant growth
and development (Philippot et al., 2013; Latz et al., 2015). Bacteria-induced plant growth pro-
motion is accomplished by several plant growth-promoting traits, viz., nitrogen fixation,
solubilization of minerals, production of hormones, siderophores, and several antimicrobial
substances to combat pathogenic attack (Kloepper et al., 1993). Cook et al. (1995) suggested
that plants may transform the microbiome of rhizosphere to their own benefit by selectively
stimulating microorganisms with PGP attributes that are beneficial to plant growth and
health.
Serratia sp. is a Gram-negative bacterium belonging to the family Enterobacteriaceae. It
has been widely known as an insect pathogen (Flyg and Xanthopoulos, 1983; Bahar and
Demirbag, 2007) and as a food-spoilage microorganism (Abdour, 2003). Different species
of Serratia were isolated from soil, water, air, and are considered opportunistic pathogens,
viz., Serratia marcescens, S. plymuthica, S. liquefaciens, S. fonticola, S. rubidaea, S. Serratia odor-
ifera, S. marnorubra, and S. proteamaculans. They secrete several virulence factors like

Beneficial Microbes in Agro-Ecology

https://doi.org/10.1016/B978-0-12-823414-3.00003-4 27 © 2020 Elsevier Inc. All rights reserved.
28 3. Serratia

chitinase, protease, DNase, lipase, hemolysin, gelatinase, chloroperoxidase, and a red

pigment prodigiosin (Kuehnert and Basavaraju, 2015). Apart from the harmful activities, it
has also been reported to stimulate plant growth by inducing resistance against plant path-
ogens (Kloepper et al., 1993), production of antimicrobial substances (de Queiroz and
de Melo, 2006), and solubilization of insoluble phosphates (Tripura et al., 2007). Phytosphere
isolates of Serratia belong to the “Serratia liquefacienseproteamaculansegrimesii’” complex
(Nakamura, 1981). It also called S. liquefaciens-like species (Grimont et al., 1982). Several
strains of these species secrete plant-growth promoting substances, antifungal metabolites,
and promote the establishment of nitrogen-fixing symbionts. Plant-associated Serratia consist
of both endophytic and free-living species in the rhizosphere. The production of indole-3-
acetic acid (IAA) by S. plymuthica AS12 and S. plymuthica AS13 may be involved in plant
growth promotion. Similarly, S. plymuthica HRO-C48 has been used as a successful biocon-
trol agent against soil-borne fungal diseases in strawberries and rapeseed (Muller et al.,
2009). S. marcescens strain 90e166 was used as potential biocontrol agent against Rhizoctonia
solani on cotton. It elicits induced-systemic resistance against diverse plant pathogens, such
as Colletotrichum orbiculare, Erwinia tracheiphila, Fusarium oxysporum, cucumber mosaic virus,
and Pseudomonas syringae pv. lachrymans (Khan et al., 2017).

2. Taxonomy of the genus Serratia

The taxonomy of the genus Serratia is still in confusion. More than 42 different species have
been associated with the genus Serratia. According to Bergey’s Manual (from the first edition to
the seventh editions), the number of different species of Serratia dropped from 23 to 5. These
five species were S. marcescens, S. plymuthicum, S. kilensis (sic), S. indica, and S. piscatorum.
Following the early work of Hefferan (1903), several taxonomists like Ewing et al.
(1959a,b), Martinec and Kocur (1960, 1961a,b,c,d), and Ewing et al. (1962) have tried to
simplify the taxonomy of red-pigmented microorganisms. The greatest simplification was
achieved by Ewing et al. (1959a,b), Ewing et al. (1962), and Martinec and Kocur (1960,
1961a,b,c,d). After simplification, Serratia became a monospecific genus.
Another species, i.e., S. marcescens var. kiliensis, was retained only because of its negative
result for Voges-Proskauer test. However, S. marcescens was the only species accepted in the
eighth edition of Bergey’s Manual of Determinative Bacteriology (Buchanan and Gibbons, 1974).
Apart from the monospecific nature of the genus, there were some evidence of other species
of Serratia that produce red pigment (Grimont, 1969; Bascomb et al., 1971; Grimont and
Dulong de Rosnay, 1972). Ewing et al. (1972, 1973) documented two species of red-
pigmented Serratia, S. marcescens and S. rubidaea. Serratia and Enterobacter ziquefaciens were
closely related, as they were sensitive to the same bacteriocins (Hamon et al., 1970). Bascomb
et al. (1971) separated Enterobacter liquefaciens to the genus Serratia.
Molecular techniques may give some evidences on the phylogenetic relationships among
enteric bacteria and may help to stipulate a particular position for the genus Serratia at a
suprageneric level. The mol% GþC content of DNAs of Serratia is usually given as
54%e60% (Colwell and Mandel, 1965; Hill, 1966). Mandel and Rownd (1964) considered
mol% GþC content of Serratia strains too heterogeneous and proposed three provisional

I. Bacteria
 3. Isolation of the genus 29
species: Serratia I (58.0e58.4), Serratia II (56.4e57), and Serratia III (53.4e55.4). Serratia III
DNA was estimated to differ from Serratia I DNA by an extra amount of 200,000 A-T nucle-
otide pairs. Serratia I corresponds to S. marcescens and identified all strains of Serratia III as
S. plymuthica (Grimont et al., 1977). Serratia II represents one strain of S. marinorubra and
some other strains of S. marcescens.
The DNA of S. marcescens has the maximum GþC content among the enteric bacteria
(Mandel and Rownd, 1964). The genome size of only one strain of S. marcescens has been
determined (Gillis et al., 1970) as 3.57  109 Da. The criterion of DNA relatedness clearly
explains that the genus Serratia is different from all known genera of the family Enterobacteri-
aceae (Steigerwalt et al., 1976).

3. Isolation of the genus

Serratia appears to be a ubiquitous genus in nature. Overall, 10 species are currently recog-
nized (Grimont and Grimont, 1992). It has been isolated from soil, water, animals (including
man), as well as from plant surfaces (Grimont and Grimont, 1992). Typical phytospheric
isolates belong to the “Serratia liquefaciens, S. grimesii” and S. proteamaculans complex (Grimont
et al., 1977), also called S. liquefaciens-like species (Grimont et al., 1982). For isolation of the
bacteria, samples were collected from the site. In the case of soil isolates, the roots along
with adherent soil part were collected from healthy plants aseptically in sterilized containers
and transported to the laboratory within an hour. Isolation of bacteria was done following
standard protocols (Purkayastha et al., 2010; Saha et al., 2012) in nutrient agar (NA)/Luria-
bertaini (LA) medium. After 72 h incubation at 30 C in inverted position, single colonies
were picked up from spread plates and pure cultures were obtained on NA slants. The strains
were subsequently maintained in NA/LA slants with periodic transfers to fresh medium. For
selective isolation of the genus Serratia, Serratia-selective medium (Ashelford et al., 2000) were
used apart from NA/LA media (Figs. 3.1 and 3.2).

FIGURE 3.1 Scanning electron micrograph of Serratia marcessens.

I. Bacteria
30 3. Serratia

FIGURE 3.2 A schematic representation of the isolation, characterization, and plant growth-promoting traits of
Serratia.

4. Characterization and identification of the genus

After isolation, the strains were characterized by different morphologic as well as biochem-
ical methods. Then the strains were identified according to Bergey’s Manual of Determinative
Bacteriology (Holt et al., 1994). The techniques for the various biochemical tests performed
followed the Benson’s Microbiological Applications, Laboratory Manual in General Microbiology
(Brown and Benson, 2007). Serratia can be differentiated from the other bacterial genera by
its production of three special enzymes: DNase, gelatinase, and lipase. It grows well on ordi-
nary microbiologic media under both anaerobic and aerobic conditions. Moreover, it grows
well on different synthetic media by modifying the carbon source. It grows well at pH 9 and
temperatures from 20 to 37 C (Giri et al., 2004). Another remarkable characteristic trait of Ser-
ratia is the production of cell-associated red color pigment, prodigiosin. The production of the
pigment, prodigiosin, is highly inconsistent among different species and is dependent on
different strains as well as the time of incubation. Prodigiosin were associated with extracel-
lular vesicles or present in intracellular granules (Matsuyama et al., 1986; Kobayashi and Ichi-
kawa, 1991). Nonpigmented strains played a significant role in causing infections (Carbonell
et al., 2000). Someya et al. (2001) observed a synergistic interaction of prodigiosin and chiti-
nolytic enzymes against spore germination of Botrytis cinerea. Nowadays, many types of dif-
ferential and selective growth media have been developed for the particular isolation and
probable testing of Serratia. For example, caprylate thallous agar was used as a selective me-
dia for Serratia. The medium contains caprylate as a carbon source and thallous salts as inhib-
itors for other microbes (Starr et al., 1976). Apart from that, the regular liquid media currently
being used for prodigiosin biosynthesis are nutrient broth (Pryce and Terry, 2000), peptone

I. Bacteria
 5. Plant growth-promoting attributes of Serratia spp. 31
glycerol broth (Montaner et al., 2000), etc. According to Nakamura, the particular economi-
cally cheap media patented by him contains 2% sodium oleate and has used only triolein
as substrate. Another media contains sesame seed powder in water. The media supplemented
with sesame seed was found to be better in terms of growth and prodigiosin biosynthesis.
Moreover, other readily available cheaper sources are used in media like peanut and coconut
(Giri et al., 2004). Sesame seed triggered the cell density in the medium, which resulted in a
higher accumulation of the intracellular positive pigment regulator by triggering excessive
pigment production. The powdered peanut seed medium supported the biosynthesis of pro-
digiosin even at 37 C. Pigment production was not detected in nutrient or peptone glycerol
broth in presence or absence of sugars (Giri et al., 2004).

5. Plant growth-promoting attributes of Serratia spp.

5.1 Biological control potential

Various rhizospheric bacteria, including B subtilis, Stenotrophomonas maltophilia, Serratia ply-
muthica, Pseudomonas fluorescens, P. trivialis, and Burkholderia cepacia produced volatile organic
compounds that inhibit mycelial growth of different fungal plant pathogens. Moreover,
quorum-sensing molecules from rhizobacteria can aggravate a range of intrinsic plant re-
sponses, including the activation of different defense-related genes (Mendes et al., 2013).
Over the last 20 years, there have been remarkable increases in the use of Serratia as biocon-
trol agent of plant diseases and therefore used as a biofertilizer (Barman et al., 2019). It was
reported that the pigment of Serratia takes part in biocontrol activity. The biosynthesis of pro-
digiosin was related to pig operon of S. marcescens ATCC274 in the SMU genome composed
of 14 genes (Harris et al., 2004). Prodigiosin has been studied to suppress growth of various
bacteria, fungi, protozoans, and also in viruses (Matteoli et al., 2018). Some isolates of
S. marcescens, S. plymuthica, S. liquefaciens, and S. entomophila have been used against different
plant pathogens. Among them, S. plymuthica seems to be the most promising biocontrol agent
(Czajkowski et al. 2012a,b). Some biocontrol strains of S. plymuthica were isolated both from
the rhizosphere as well as from the internal tissues of many crop plants (Benhamou et al.,
2000; Czajkowski et al. 2012a,b). S. plymuthica A30 was helpful in controlling blackleg and
soft rot disease in Solanum tuberosum caused by Dickeya sp. IPO3012. Blackleg incidence
was reduced from 55% in the control Dickeya sp.-inoculated treatment to 0%. The disease inci-
dence was reduced by 100% and the prevalence of stem colonization was cut down by 97%
(Czajkowski et al. 2012a,b) when seed tubers were vacuum coinfiltrated with Dickeya spp.
and high concentration of S. plymuthica A30 and then planted in the compost. Some strains
of S. plymuthica were reported to induce systemic resistance in several crops: S. plymuthica
R1GC4 stimulated defense mechanisms against fungal pathogens in Cucumis sativus
(Benhamou et al., 2000), and S. plymuthica IC270 induced defenses of Oryza sativa against
the blast pathogen Magnaporthe oryzae (De Vleesschauwer et al., 2009). S. plymuthica
IC1270, isolated from the rhizospheric soil of Vitis vinifera, controlled the pathogenic attack
of Rhizoctonia solani on bean and cotton and Pythium aphanidermatum in cucumber (De
Vleesschauwer et al., 2009). S. plymuthica 3Re4-18 was used for preservation of potato sprouts
against the effect of R. solani. S. plymuthica HRO-C48 was effective against R. solani, Sclerotinia

I. Bacteria
32 3. Serratia

sclerotiorum, and Verticillium dahliae (Muller et al., 2009). Some strains of S. plymuthica effec-
tively controlled air-borne fungal plant pathogens; S. plymuthica G15 showed antifungal
activity against Botrytis cinerea and S. plymuthica strains IC14 and IC1270 against Penicillium
italicum and P. digitatum (Muller et al., 2009). Apart from that, some strains of S. plymuthica
was found to control bacterial plant pathogens. S. plymuthica IC1270 successfully inhibited
crown gall of Lycopersicum esculentum caused by Agrobacterium tumefaciens and A vitis
(Muèller and Berg, 2008).

6. Phytoremediation

Nowadays, microbe-mediated phytoremediation has emerged as a more successful

approach for the remediation of heavy metalecontaminated soils. Many Serratia sp. exhibit
tolerance to heavy metals and have phytoremedial consequences on host plants (Khan
et al., 2015; Luo et al., 2011; Wan et al., 2012). An endophytic strain of Serratia nematodiphila
LRE07 has been isolated from Solanum nigrum (Luo et al., 2011). S. marcescens RSC-14 was iso-
lated from the same plant rhizosphere as the hyperaccumulator of Cd as it harbors
Cd-tolerant genes. The Cd and other heavy metaleresistant genes in the genome of RSC-
14 might be engaged in Cd uptake, accumulation, and detoxification within the cell.
Low-level resistance to heavy metals is accomplished by binding the metal ions in the inac-
tive form nonspecifically to the cell wall to prevent toxic effects in the cell. Several antioxidant
enzymes, viz., catalase, superoxide dismutase, and glutathione peroxidase, and reduced
glutathione produced by the strain may allow the plants to tolerate detoxification and alle-
viate oxidative stress caused by intracellular Cd accumulation (Khan et al., 2015, 2017).
Serratia sp. SY5 increased the biomass of root under Cd-contaminated environments. So
the strain SY5 could be used as an effective inoculant for phytoremediation in toxic heavy
metalepolluted soil (So-Yeon and Cho, 2009).

6.1 Other plant growth-promoting activities

Apart from the biologic control potential and phytoremediation, several other PGP activ-
ities were reported by several workers. The other PGP activities include P- and Zn solubili-
zation, secretion of lytic enzymes, siderophore production, IAA production, etc. Some of
the PGP activities by different species of Serratia are now described.
The expression and secretion of lytic enzymes like chitinase, cellulase, protease, and DNase
produced by soil bacteria also results in direct suppression of pathogenic activities by hydro-
lyzing several polymeric compounds (Kumar et al., 2005; Someya et al., 2001; Muller et al.,
2009). Chitinase from soil microorganisms and some plants takes part in a defense mecha-
nism (Liu et al., 2003). It was very proficient in depolymerization of chitin because of its
ability to produce different chitinolytic enzymes (Brurberg et al., 1995). Although, chitinase
production and its activity depends on several physical and growth conditions, viz., culture,
pH, temperature, etc. Furthermore, bacterial siderophores play a major role in plant disease
suppression by iron sequestration since fungal siderophores have lower affinity toward iron
available in soil (Compant et al., 2005; Berg, 2009). S. marcescens strain ETR17 isolated from
tea rhizosphere was found to produce lytic enzymes, HCN, siderophores, and IAA (Dhar

I. Bacteria
 References 33
Purkayastha et al., 2018). The strain also produced some amount of IAA, thereby promoting
plant growth. Serratia is one of the most potent producers of chitinases, whose production,
gene regulation, and activity were well characterized (Gutierrez-Roman et al., 2014). Purified
chitinases from S. proteamaculans (Mehmood et al., 2009), S. plymuthica (Frankowski et al.,
2001), and S. marcescens (Wang et al., 2013) exhibited antifungal activity against different
pathogenic fungi. S. marcescens SR1 produced chitinase and thus is used as a biocontrol agent.
The one ml cell free supernatant of the strain was effective against F. oxysporum, Sclerotium
rolfsii, Rhizoctonia solanii, and Alternaria alternata up to 60.0%e73.3% (Parani et al., 2011).
Nitrogen phosphate (P) is considered one of the major macroelements for growth and
development of crop plants. But most of the soil P is unavailable to the plants because it is
complexed with several cations like Ca, Mg, Fe, and Al soil for its low solubility (Ghosh
et al., 2019). P is mostly present in poorly soluble mineral phosphates that are not readily
available for plant uptake (Ghosh et al., 2016). Soil microbes played a key role in phosphate
solubilization. Microbial conversion of insoluble mineral P forms into soluble ionic phosphate
(H2PO 4 ) is a key mechanism of release of the bound P (Alori et al., 2017). Moreover, forma-
tion of biofilm on the P granules plays a major role in P solubilization processes (Ghosh et al.,
2019). S. marcescens UENF-22GI (SMU) was able to solubilize inorganic P and Zn. The strain
also forms biofilms and thereby helps in P and Zn solubilization processes. Biofilm-forming
capability of the strain inhibits two strains of phytopathogenic Fusarium species (Matteoli
et al., 2018).

Acknowledgment
Authors were thankful to SERB- National Post-Doctoral Fellowship (File Number: PDF/2017/002639) for financial
assistance.

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