Introduction

Marine organisms are well known to have specific rela-tionship with numerous microorganisms with no excep-tion to sponges. The relationships of marine sponges and marine microorganisms that may serve as food or that live either permanently or temporarily are highly complex and far from being understood (Wilkinson, 1992; Steindler et al., 2005). It seems that sponges have likely hosted associated microorganisms since the first appearance of the phylum over 500 million years ago (Wilkinson, 1984). Sponges are filter feeders and during the feeding process the bacteria from the environment are continuously swirled in by the sponge driven currents and most of these bacteria are retained in the sponge body (Thakur et al., 2004). The associates are located both intracellularly and extracellularly (Vacelet and Donadey, 1977; Wilkinson, 1992). Some communities are on the outer layers of sponges (Haygood et al., 1999) and some permanently reside in the sponge mesohyl, pointing to the close interaction between the host and associated bacteria (Webster and Hill, 2001; Friedrich et al., 2001; Bohm et al., 2001). The amount of microbial communities

residing in sponges varies between host sponges. The sponges can host a variety of microbes, including cyano-bacteria (Vincente, 1990; Arillo et al., 1993; Magnino et al., 1999), diverse heterotrophic bacteria (Wilkinson 1978a, b, c; Santavy et al., 1990; Magnino et al., 1999), unicellular algae (Sara and Liaci, 1964; Rützler, 1988; Wilkinson, 1992), fungi (Holler et al., 2000; Webb and Maas, 2002), and zoochlorellae (Gilbert and Allen, 1973). In some species of sponges, microorganisms can account for up to 60% of the sponge biomass (108–1010 bacteria per gram of sponge wet weight) (Wilkinson, 1978 a, b, c), exceeding seawater concentrations by two to three orders of magnitude (Friedrich et al., 2001). Such sponges have been termed as bacteriosponges or high microbial abun-dance sponges (Vacelet and Donadey, 1977; Hentschel et al., 2003). However the mesohyl of other sponges that coexist in the same habitat are devoid of microorganisms (low microbial abundance sponges).

Because sponge-microbe associations are widely distributed across sponge taxa and, in some cases, are unique to sponges (Hentschel et al., 2002, 2006), many of these associations are thought to be truly mutualistic rather than transient associations resulting from sponge

Critical Reviews in MicrobiologyCritical Reviews in Microbiology, 2010; 36(1): 82–90

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Address for Correspondence: Joseph Selvin Marine Bioprospecting Laboratory Department of Microbiology Bharathidasan University, Tiruchirappalli 620024, India. Tel: 91-431-2407082 Fax: 91-431-2407045; Email: selvinj@rediffmail.com, jselvin@bdu.ac.in

03 July 2009

04 October 2009

08 October 2009

1040-841X

1549-7828

© 2010 Informa UK Ltd

10.3109/10408410903397340

R E V I E W A R T I C L E

Sponge-microbial interactions: Ecological implications and bioprospecting avenues

Joseph Selvin*,1, A.S. Ninawe2, G. Seghal Kiran1, and A.P. Lipton3

1School of Life Sciences, Bharathidasan University, Tiruchirappalli 620024, India, 2Maharashtra Animal & Fishery Sciences University, Nagpur, Maharashtra - 440006 India, and 3Central Marine Fisheries Research Institute, Vizhinjam 695521, Thiruvananthapuram, India

AbstractSponges are closely associated with microorganisms that occur either intracellularly and extracellularly. Sponges are soft-bodied sessile organisms appear to be defenseless in facing predation. Microbial symbionts supposed to have a functional role in the host defense against pathogens, predation and microfouling proc-esses. Recently, the ubiquitous defense enzyme, phospholipase A2 (PLA2) detected in the sponge associated bacterium envisaged the possible functional role in the ecological succession of host sponge against preda-tory / fouling pressure in the habitat. In present review, we highlighted the possible functional interactions between associated microbes and host sponges and its potentials in bioprospecting approaches.

Keywords: Marine-sponge; sponge-bacteria; microbial-association; sponge-microbial interactions; bioprospecting; chemical ecology

MBY

439912

(Received 03 July 2009; revised 04 October 2009; accepted 08 October 2009)

ISSN 1040-841X print/ISSN 1549-7828 online © 2010 Informa UK LtdDOI: 10.3109/10408410903397340 http://www.informahealthcare.com/mby

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Sponge-Microbial Interactions: Ecological Implications and Bioprospecting Avenues 83

filter feeding activity (Preston et al., 1996; Fuerst et al., 1999; Haygood et al., 1999). Although sponge microbe interactions can be characterized under different head-ings (Figure 1), the symbioses particularly the endosymbi-onts of marine sponges remains to be a triumphant focus of research. Thus physiological and ecological roles have been ascribed to sponge microbial endosymbionts. These include nutritional enhancements (Wilkinson, 1992; Arillo et al., 1993; Vacelet et al., 1996), stabilization of the sponge skeleton (Wilkinson et al., 1981), and secondary metabolite production (Unson et al., 1994; Bewley et al., 1996; Schmidt et al., 2000). There are numerous reviews which points on the sponge microbe interactions in vari-ous aspects. Our review is unique on the core focus that the physiological and ecological roles of these microbes have been linked to the biotechnological prospecting of sponge-associated microbes. The present review aims to elucidate the significance of sponge-microbial inter-actions on bioprospecting approaches. In addition to the hypotheses, findings and theories drawn from the published reports, deliberations were emphasized with preliminary findings from our laboratory.

Mechanism of host sponge-microbe interaction

Unlike the prominent squid-luminescent bacte-rium symbiosis, the molecular basis of the symbiotic

relationship between sponge and microorganism has not been defined. However, the generalized molecular mechanism of marine invertebrate-microbial associa-tion can be analogized certain extent for understanding the specialized features of sponge-microbial associa-tion. Once the symbiotic microorganisms arrive at the specific point of colonization, the host presents condi-tions that permit the organism to recognize this site and be retained there (Figure 2). The selective process is likely to be mediated by receptor ligand interactions through highly specific immunological cross-reactions as observed by the antigens agglutination reactions. From a previous study (Muller et al., 1979), it is known that a lectin in the Geodia sponge system controls the aggregation potency of the sponge cells. The biologi-cal role of the sponge lectins might not be restricted to reaggregation processes alone, but also might have an additional biological function, the maintenance of a symbiosis between a marine sponge (H. panicea) and a bacterium (P. insolita) (Muller et al., 1981). There are also evidences where surface glycans function to recognize the specific symbiotic microorganism and facilitate their maintenance (McFall-Ngai and Ruby, 1994). Further experiments suggested the recognition of particular microorganism—by the host sponge—can be possible through the mechanism of antibiosis. This biological system is based on the ability of some bacteria to adapt to the presence of antibiotics produced by the host. Once the bacteria have established themselves in their target

Sponge-microbialinteractions

Mutualism(+/+)

Antibiosis(+/0)

Defense enzymes(+/0)

Pathognesis(−/0)

Symbiosis(+/+)

Signaling molecules(+/+)

Co-synthesis(+/+)

Co-metabolism(+/+)

Microfouling(−/+)

Sponge Microbes

Bioprospecting avenues

Culturable microbes

Production ofsecondarymetabolites

Expression of synthansin surrogate host

Functional metagenomicsand diversity

Unculturablemicrobes

Microbial

Diversity

Figure 1. The hypothetical mechanism of interaction and approaches in exploring the sponge associated microbes.

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tissues, both the host and the microorganism change from an initiation mode to a persistence mode. The bacteria induce significant remodeling including apop-tosis induced by lipopolysaccharide (Foster et al., 2000). Once inside the host sponge if the microbe encounters favorable conditions (e.g., high nutrients), it may mul-tiply through physical enrichment obtained near the choanocyte chambers due to the sponge’s filtering activities. There are also evidences for the production of quorum sensing signaling molecules (e.g., N-acyl homo-serine lactone, AHLs) produced by Alpha- and Gamma-proteobacteria isolated from marine sponges Mycale laxissima and Ircinia strobilina) through which the best survived microbial community out-compete other potential colonizers and establish themselves within the sponge tissue. Apart from this mode of colonization it has been predicted that a subtractive enrichment occurs, whereby those microbes which cannot resist phagocyto-sis by sponge cells are consumed (Wilkinson, 1984).

Group living

The relation between sponges and microbes can be considered as a behavioral ecology of animals living in groups. When this is considered then a central question arises why they live in groups (Krause and Ruxton, 2002). The hypothesized benefits obtained from group living include, but are not limited to, decreased risk of preda-tion, increased feeding or foraging efficiency, improved defense of resources, and help in rearing offspring (Alexander, 1974; Wilson, 1975; Trivers, 1985).

Sponges, being soft-bodied sessile organisms, appear to be defenseless in facing predation. Despite these intense predation on tropical reefs by few fish species (Randall and Hartman, 1968; Wulff, 1994, Dunlap and Pawlik, 1996), Hawsbill turtles (Meylan, 1988), Nudibranchs (Thompson, 1982), Echinoderms (Dayton 1989), sea urchins (Vance, 1979; Ayling, 1989), the limited number of sponge predators along the reefs is especially surprising (Hay, 1991). The question thus arises: How do reef sponges defend themselves against predation. The chemical or a physical defense mechanism can prevent these animals from predation. The presence of spicules, spongin, and low nutritional quality of tissue can constitute a physical anti-predatory defense mechanism. The studies on the contribution of these mechanisms in defense against predation concluded that chemical defense, rather than physical defense or low nutritional quality, was the most important defensive mechanism used by sponges (Chanas and Pawlik, 1995; Burns et al., 2003).

Antipredatory activity of endosymbionts

Thus a possible antipredatory function can be given to the endosymbionts of marine sponges. Endosymbionts can provide protection against pathogens and, together with host immune systems, provide their hosts with a complex integrated defense against pathogens (Kitano and Oda, 2006). Savage (1977) and Tannock (1995) reviewed some of the mechanisms by which endosymbionts interfere with the colonization of their hosts by potential pathogens. These includes, (a) the

Colonization ofsymbiotic microbes

Attraction of specificsymbionts towards host

Presentation of recognitionsites for the symbionts

Production ofsignaling molecules

Inside the host cells themicrobes encounter favorable

conditions for their growth

Survival of the organismsafter subtractive enrichment

MECHANISM OF SPONGE-MICROBEINTERACTION

Establishment ofsymbiotic colonies

Figure 2. The possible mechanism of sponge-microbe interaction.

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Sponge-Microbial Interactions: Ecological Implications and Bioprospecting Avenues 85

endosymbionts may ecologically out-compete (i.e., the competitive exclusion principle) pathogens for space and nutrients, (b) endosymbionts produce bacteriocins that are toxic to other microbes (Daw and Falkiner, 1996), (c) endosymbionts may parasitize larger microbial invaders. (d) Invading microbes may be preyed upon by endosymbionts (e) endosymbionts may alter host physiology, making it difficult for invading pathogens to become established (e.g., Falk et al., 1998; Hooper et al., 1998, 2001, 2003; Stappenbeck et al., 2002) and (f ) endosymbionts may prime the immune system, preparing it for rapid responses when it is exposed to pathogens in the future.

Of these, the chemical defenses significantly influence the outcomes of diverse inter and intraspecific interactions in both terrestrial and marine environments (Feeny, 1991; Pawlik, 1993; Hay, 1996; McClintock and Baker, 1997). Secondary metabolites can deter consumers and com-petitors, as well as inhibit the growth of pathogens, and thus affect community structure and function (Hay, 1996; McClintock and Baker, 1997). Recent research has begun to highlight another type of “complex” system potentially of great importance to the field of chemical ecology: microbial symbiont production of bioactive secondary metabolites that contribute significantly to host survival.

Defensive enzymes from endosymbionts

Apart from secondary metabolites, the symbionts pro-duce defense enzymes, phospholipases as a first line of defense. The evidence for this came from the work carried out in our laboratory (Selvin, 2009). The results proved that another possible defense mechanism in this sessile organism can be the production of an extracel-lular enzyme phospholipase A2 (PLA2). The PLA2 is a ubiquitous defense enzyme found in snake and bee ven-oms and distributed throughout the plant and animal kingdom (Stahl et al., 1999). Recent studies envisaged that varying levels of PLA2 was found in marine inver-tebrates including Cnidaria (Nevalainen et al., 2004a), Porifera (Nevalainen et al., 2004b) and Echinodermata. But the PLA2 in sponge associated bacteria has not been reported so far. The attempt to explore the possible func-tional role of PLA2 synthesis in sponge associated bacteria revealed that the host sponge and the associated isolate Streptomyces dendra sp. nov. MSI051 yielded more or less similar phospholipase A2 activity. Thus the enzyme may have key functional role in the ecological succession of host against predatory / fouling pressure in the habitat.

Similar secondary metabolite profile

Over the past decade, there has been a growing awareness that secondary metabolites isolated from marine sponges may actually be produced by a symbiont (Vacelet and

Donadey, 1977; Wilkinson et al., 1981). This idea was ini-tially proposed based on the isolation from marine inver-tebrates of compounds structurally similar or identical to compounds previously reported from microorganisms (Anthoni et al., 1990; Kobayashi and Ishibashi, 1993). The physical separation of symbiont cells from host tissues has provided more direct evidence for symbiont production of some metabolites (e.g., Faulkner et al., 1999) and, in a few instances, microorganisms cultured from host mate-rial have produced compounds identical to those isolated from the host (Stierle et al., 1988; Elyakov et al., 1991).

Several reasons can be put forth in order to justify the presence of similar secondary metabolites both in sponges and associated bacteria. These include the genes involved in the biosynthetic pathway of secondary metabolites may occur as a whole either in the sponge or in the microbial associate. Integration of host and sym-biont genomes was discussed by Sara et al. (1998). As a result of symbiosis it can be hypothesized that the gene for the biosynthetic pathway that resides in the associ-ate microbe integrates with the host sponge genome resulting in a potential reduction of microbial genome size as reported for many obligate insect endosymbi-onts (Nakabachi et al., 2006; Zientz et al., 2004). The vice-versa integration can also occur thus resulting in a combinatorial biosynthesis of novel lead compounds. But it is unknown whether such tight host-symbiont coupling occurs in sponges limiting this reason at its infancy. Another added reason can be the presence of a mechanism of co-synthesis of secondary metabolites by both the sponges and associated microbes. The product formed as a result of biosynthetic pathway (sponge/bac-teria) acts as a precursor for another (bacteria/sponge) resulting in a new-fangled secondary metabolite. And according to the optimal defense theory first suggested by McKey (1974), secondary metabolites may be pro-duced by the microbe and concentrated in the vulner-able body parts that are first encountered by predators (Avila and Paul, 1997; Gillor et al., 2000).

Tapping the untapped

Thus the enormous reserve of secondary metabolites from these endosymbionts can be tapped for human welfare with a new insight of exploring organisms from pristine habitats as sources of novel bioactive secondary metabolites. The response for this view is at its peak because the rate of dis-covery of new compounds from terrestrial organisms has decreased, whereas the rate of reisolation of known com-pounds has increased. Moreover as marine environmental conditions are extremely different from terrestrial ones it is surmised that marine organisms have different character-istics from those of terrestrial counterparts and therefore might produce different types of bioactive compounds. The

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list of compounds in Table 1 is exclusively from microbes associated with marine sponges.

Particularly sponge associated actinobacteria needs special mention in the production of broad range of antimicrobials. The sponge-associated marine actino-mycetes showed potential antimicrobial activity against human pathogens. The antagonistic producers including Saccharamonospora CPI3, Saccharamonospora CPI9, Micromonspora CPI12, Streptomyces CPI13 isolated from the marine sponge Callyspongia diffusa showed high-est antimicrobial activity (Gandhimathi et al., 2008). 11 compounds with antimicrobial activity were isolated from Nocardiopsis dassonvillei MAD08, an endosymbiont of host sponge D. nigra which was cultured under laboratory condition. This is the first strain that produce both organic solvent and water soluble antimicrobial compounds. The active extract was non-hemolytic and showed surface active property envisaging its probable role in inhibiting the attachment of pathogens to host tissues thus blocking host-pathogen interaction at an earlier stage of pathogen-esis. The isolate Nocardiopsis MAD08 also produced an 87.12 kDa anticandidal protein (Selvin et al., 2009).

Thus these symbionts can be cultured in bioreactors providing optimal conditions for its growth and produc-tion of secondary metabolites in order to mitigate the sufferings of humans. But in spite of all these success, the cultivation fritters away as the isolate fails to produce the necessary compound anymore. Additionally, and for unknown reasons, some bacteria simply stop producing the compound of interest after a certain time on artificial media. This could be due to any of a number of genetic reasons relating to a lack of selective pressure in pure cul-ture, e.g., point mutation in a key gene or loss of a mobile genetic element carrying the biosynthesis genes. So there is an urgent need for enormous more studies to be carried out to achieve success in this field for flawless production of pharmaceuticals from the nature selected microbes.

Enhancement of nutrition uptake: Endosymbionts are the reservoir of digestive enzymes?

Sponges swirl in a large volume of seawater contain-ing organic particles. Hence, it is reasonable to believe

that some microbes in sponges produce hydrolytic enzymes to convert these organic matters into nutri-ents. Therefore, endosymbionts act on complex organic matter and converts them into easily acces-sible sources, thus playing a nutritional role for the host sponge. Evidences for this come from the study of enzyme production by various microbes isolated from marine sponges. Species of the bacterial genus Cytophaga can hydrolyze agar and were identified from the sponge Halichondria panacea (Imhoff and Stoher, 2003). Bacteria isolated from six marine sponges (Spirastrella sp., Phyllospongia sp., Ircinia sp., Aaptos sp., Azorica sp., and Axinella sp.) were identified to produce amylase, carboxymethylcellulase, and pro-teases (Mohapatra et al., 2003). Further supporting evidences comes from our laboratory where cultivable sponge associated endosymbionts from two marine sponges, Fasciospongia cavernosa and Dendrilla nigra has shown to produce nutritionally valuable enzymes including amylase, protease, lipase, and cellulase (Shanmughapriya et al., 2008; Shanmughapriya et al., 2009; Kiran et al., 2008).

Ecology and physiology in respect to urea hydrolysis

The outcome of the primary screening for enzyme producers was fascinating as nearly 65% of the isolates showed positive production of urease at a very early stage of their growth, i.e., in the early log phase. From these it can be hypothesized that the sponge would have been exposed to an area contaminated with urea that is toxic to sponges. When the high effectiveness of urea hydrolysis by these endosymbionts are considered at the ecological aspects as the microbes associated with the sponges utilize urea and convert them into ammo-nia which enters into nitrogen cycle thus maintaining the nitrogen level of the atmosphere. Moreover when the benefits for sponges by these urea utilizing bacteria are considered they enhance protein synthesis in the host sponge by breaking down urea to ammonia. Thus these microbes can play a potential nutritional, physi-ological and ecological role in the host sponge and the surrounding environment.

Table 1. List of sponge compounds isolated from the sponge-associated microbes.

Bioactivity Compound Associated microbes Reference

Phosphatase inhibitor Okadaic acid Prorcentrum (dinoflagellate) Murakami et al., 1982

Anticancerous Demethylisodysidenin Oscillatoria spongeliae(cyanobacteria) Berthold et al., 1982

Antifungal Theopalaumide (peptide) Entotheonella palauensis(Filamentous bacteria)

Bewley et al., 1996 Schmidt et al., 2000

Cytotoxic Swinholide Proteobacteria Bewley and Faulkner, 1998

Cytotoxic Chondramide D and Jasplakinolide

Jaspis sp. Crews et al., 1986; Zabriskie et al., 1986

Cytotoxic Sorbicillactone A Pencillium chrysogenum Bringmann et al., 2003

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Success story for large scale production of enzymes

Thus the production of the above mentioned enzymes have been exploited in vitro conditions and successful production of alkalophilic amylase from Halobacter MMD047 (Shanmughapriya et al., 2009), psychrophilic alkaline lipase of Pseudomonas (Kiran et al., 2008), thermotolerant alkaline protease of Roseobacter MMD040 (Shanmughapriya et al., 2008), alkaline cel-lulase of Marinobacter MSI032 (unpublished data), thermostable amylase of Nocardiopsis dassonveille MAD04 (unpublished data) have been achieved. These enzymes apart from having a nutritional role can also find wide applications in the manufacture of pharma-ceuticals, foods, beverages, confectionary, detergents, as well as in textile and leather processing and waste water treatment.

Not only industrially useful enzymes are produced from sponge associated bacteria but evidences are avail-able for the production of clinically relevant enzymes. The bacterium Arthrobacter ilicis and fungus Mucor sp. isolated from the sponge Spirastrella sp. were found to produce an acetylcholinesterase and amylase, respec-tively (Mohapatra and Bapuji, 1997; Mohapatra et al., 1998). These two enzymes were heat-tolerant and their activities not affected by the major cations of seawater, such as Na+, Ca2+, and Mg2+, at relatively high concentra-tions. Finally, the bacterium Micrococcus sp. associated with the Spirastrella sponge produced urethanase, which could potentially be used to remove urethane, a cancer-causing chemical, from alcoholic beverages (Margot et al., 2002).

Pelleted/ encapsulated endosymbionts, a boon to uremic patients

The urease producing potentials of the sponge associated microbes can be exploited in a novel way for pharmaceu-tical applications. Live microorganisms that are urease positive can be pelleted/ encapsulated as done for pro-biotic strains and supplemented for uremic patients. As a result of this supplementation the frequency of dialysis is expected to be reduced greatly thus increasing life span of the patients. It has been hypothesized that probiotic bacteria instilled into the gastrointestinal tract could help in converting nitrogenous wastes accumulated due to renal insufficiency into nontoxic compounds; thereby, ameliorating the biochemical imbalance. Therefore the sponge-associated endosymbionts can be developed as potential probiotic pellets. This hypothesis has already been proposed for the development antagonistic probi-otics to prevent mid-culture outbreaks in shrimp aqua-culture (Selvin and Ninawe, 2009).

Bioindicators and bioremediation—a new claim

It has been reported that the sublethal exposures to heavy metals may affect the physiological functions and behavior of organisms without killing them. So when sponges are exposed to heavy metal pollution, they are at the risk of damage that may be lethal to the sponges. Thus some defense mechanism should come into act to prevent these sponges from adverse effects. Selvin et al. (2009) established that the effect of heavy metal pollu-tion in the habitat could be detected directly from the sponge-associated bacteria instead of in situ monitoring of host sponges for behavioral changes. The sponge-as-sociated bacteria might be an ideal bioindicator model for monitoring of heavy metal pollution in marine habi-tats. These associated bacteria seem to be highly toler-ant to various concentrations of different heavy metals. So it can be suggested in an another way around that the endosymbionts of marine sponges exposed to heavy metal toxicity can act on these contaminants and turns them to be non-toxic and thus reducing the risk to host sponges. Thus with this perspective utilization of these strains for bioremediation of heavy metals can open up a new pioneering gateway for the development of more efficient microorganisms that can find its application in the field of environmental biotechnology. Further the application of these endosymbionts can make them to hold a new position in the database of organisms used for increased oil recovery and also in bioremediation of oil spills as these microbes showed increased bio-surfactant and bioemulsification activity (Gandhimathi et al., 2009: Kiran et al., 2009).

Conclusion

Despite the advances in demonstrating a microbial origin for a growing number of secondary metabolites isolated from diverse marine invertebrates, we know of very few published examples for which an ecological role has been identified for a symbiont-produced marine secondary metabolite. Unto our knowledge, there is no demonstrated evidence available on the anti-predatory chemical defense of microbial symbionts and/or inte-grated chemical defense of sponge-microbial associa-tion. Thus even though hypothesis and conclusions are being drawn about the origin of secondary metabo-lites, the disclosure unique ecological phenomenon of sponge-microbial association is inevitable to explore the unseen microbial majority for bioprospecting approaches. Thus the full potency of the microorgan-isms has to be tapped for maximum utilization of the resources. In addition, the enzymes produced by the sponge associated microbes are being ignored greatly

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and thus it continues to be in its infancy. Researchers and investigators should turn their attention towards the production of such valuable industrial and pharmaceu-tical enzymes. The remuneration obtained from these endosymbionts needs to be explored for biotechnologi-cal potentials. The hypothesized benefits obtained by group living and the implications of these in prospect-ing human life has been highlighted in this review. Thus a relation between marine and terrestrial habitats has been drawn with a new insight.

Declaration of interest: JS thanks the Department of Biotechnology (DBT), New Delhi for financial support under Rapid Grant for Young Investigators. This paper is an outcome of the ongoing DBT-RGYI funded project.

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