Article

Sponge-Associated Microorganisms: Evolution, Ecology, and Biotechnological Potential

Department of Microbial Ecology, University of Vienna, Althanstr. 14, A-1090 Vienna, Austria.
Microbiology and Molecular Biology Reviews (Impact Factor: 14.61). 07/2007; 71(2):295-347. DOI: 10.1128/MMBR.00040-06
Source: PubMed

ABSTRACT

Marine sponges often contain diverse and abundant microbial communities, including bacteria, archaea, microalgae, and fungi. In some cases, these microbial associates comprise as much as 40% of the sponge volume and can contribute significantly to host metabolism (e.g., via photosynthesis or nitrogen fixation). We review in detail the diversity of microbes associated with sponges, including extensive 16S rRNA-based phylogenetic analyses which support the previously suggested existence of a sponge-specific microbiota. These analyses provide a suitable vantage point from which to consider the potential evolutionary and ecological ramifications of these widespread, sponge-specific microorganisms. Subsequently, we examine the ecology of sponge-microbe associations, including the establishment and maintenance of these sometimes intimate partnerships, the varied nature of the interactions (ranging from mutualism to host-pathogen relationships), and the broad-scale patterns of symbiont distribution. The ecological and evolutionary importance of sponge-microbe associations is mirrored by their enormous biotechnological potential: marine sponges are among the animal kingdom's most prolific producers of bioactive metabolites, and in at least some cases, the compounds are of microbial rather than sponge origin. We review the status of this important field, outlining the various approaches (e.g., cultivation, cell separation, and metagenomics) which have been employed to access the chemical wealth of sponge-microbe associations.

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    • "Interestingly, marine sponge can form close associations with the symbiotic microbial communities within their bodies (Taylor et al., 2007), and thus, the symbiotic microbial community is sponge-specific and distinct from those in the surrounding seawater and other habitats (Taylor et al., 2007; Lee et al., 2011). Symbiotic microorganisms play essential roles in the sponge body, participating in carbon, nitrogen, and sulfur cycles (Taylor et al., 2007). "
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    ABSTRACT: Glass sponge (Hexactinellida, Porifera) is a special lineage due to its unique tissue organization and skeleton material. Structure and physiology of glass sponge have been extensively studied. However, our knowledge of the glass sponge-associated microbial community and the interaction with the host is rather limited. Here, we performed genomic studies on the microbial community in the glass sponge Lophophysema eversa in seamount. The microbial community was dominated by an ammonia-oxidizing archaeum (AOA), a nitrite-oxidizing bacterium (NOB) and a sulfur-oxidizing bacterium (SOB), all of which were autotrophs. Genomic analysis on the AOA, NOB and SOB in the sponge revealed specific functional features of sponge-associated microorganisms in comparison to the closely related free-living relatives, including chemotaxis, phage defense, vitamin biosynthesis and nutrient uptake among others, which are related to ecological functions. The three autotrophs play essential roles in the cycles of carbon (C), nitrogen (N) and sulfur (S) in the microenvironment inside the sponge body, and they are considered to play symbiotic roles in the host as scavengers of toxic ammonia, nitrite and sulfide. Our study extends knowledge regarding the metabolism and evolution of chemolithotrophs inside the invertebrate body.
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    • "However, the composition and function of microbial community of glass sponges from deep sea are largely unknown. Because of the well-known host species specificity of microbial community in sponges (Taylor et al., 2007), the microorganisms in glass sponges are supposed to be unique to those from other sponges and free-living relatives in terms of function and evolution. Here we perform studies on the microbial community and microbial genomes of deep-sea glass sponge Lophophysema eversa, and provided insights into the ecological function of the potential microbial symbionts in the sponge. "
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    ABSTRACT: Glass sponge (Hexactinellida, Porifera) is a special lineage due to its unique tissue organization and skeleton material. Structure and physiology of glass sponge have been extensively studied. However, our knowledge of the glass sponge-associated microbial community and the interaction with the host is rather limited. Here, we performed genomic studies on the microbial community in the glass sponge Lophophysema eversa in seamount. The microbial community was dominated by an ammonia-oxidizing archaeum (AOA), a nitrite-oxidizing bacterium (NOB) and a sulfur-oxidizing bacterium (SOB), all of which were autotrophs. Genomic analysis on the AOA, NOB and SOB in the sponge revealed specific functional features of sponge-associated microorganisms in comparison to the closely related free-living relatives, including chemotaxis, phage defense, vitamin biosynthesis and nutrient uptake among others, which are related to ecological functions. The three autotrophs play essential roles in the cycles of carbon (C), nitrogen (N) and sulfur (S) in the microenvironment inside the sponge body, and they are considered to play symbiotic roles in the host as scavengers of toxic ammonia, nitrite and sulfide. Our study extends knowledge regarding the metabolism and evolution of chemolithotrophs inside the invertebrate body.
    Full-text · Article · Nov 2015 · Environmental Microbiology
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    • "As one of the oldest multicellular animals (Love et al., 2009), marine sponges (phylum Porifera) often harbor dense and diverse microbial communities, and the sponge-microbe associations represent one of the most complex symbioses on earth (Taylor et al., 2007). Actinobacteria are commonly found in association with sponges (Simister et al., 2012). "
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    ABSTRACT: Marine sponges often harbor dense and diverse microbial communities including actinobacteria. To date no comprehensive investigation has been performed on the culturable diversity of the actinomycetes associated with South China Sea sponges. Structurally novel aromatic polyketides were recently discovered from marine sponge-derived Streptomyces and Saccharopolyspora strains, suggesting that sponge-associated actinomycetes can serve as a new source of aromatic polyketides. In this study, a total of 77 actinomycete strains were isolated from 15 South China Sea sponge species. Phylogenetic characterization of the isolates based on 16S rRNA gene sequencing supported their assignment to 12 families and 20 genera, among which three rare genera (Marihabitans, Polymorphospora, and Streptomonospora) were isolated from marine sponges for the first time. Subsequently, β-ketoacyl synthase (KSα) gene was used as marker for evaluating the potential of the actinomycete strains to produce aromatic polyketides. As a result, KSα gene was detected in 35 isolates related to seven genera (Kocuria, Micromonospora, Nocardia, Nocardiopsis, Saccharopolyspora, Salinispora, and Streptomyces). Finally, 10 strains were selected for small-scale fermentation, and one angucycline compound was detected from the culture extract of Streptomyces anulatus strain S71. This study advanced our knowledge of the sponge-associated actinomycetes regarding their diversity and potential in producing aromatic polyketides.
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