Abstract

Marine sponges harbour complex microbial communities of ecological and biotechnological importance. Here, we propose the application of the widespread sponge family Irciniidae as an appropriate model in microbiology and biochemistry research. Half a gram of one Irciniidae specimen hosts hundreds of bacterial species—the vast majority of which are difficult to cultivate—and dozens of fungal and archaeal species. The structure of these symbiont assemblages is shaped by the sponge host and is highly stable over space and time. Two types of quorum-sensing molecules have been detected in these animals, hinting at microbe-microbe and host-microbe signalling being important processes governing the dynamics of the Irciniidae holobiont. Irciniids are vulnerable to disease outbreaks, and concerns have emerged about their conservation in a changing climate. They are nevertheless amenable to mariculture and laboratory maintenance, being attractive targets for metabolite harvesting and experimental biology endeavours. Several bioactive terpenoids and polyketides have been retrieved from Irciniidae sponges, but the actual producer (host or symbiont) of these compounds has rarely been clarified. To tackle this, and further pertinent questions concerning the functioning, resilience and physiology of these organisms, truly multi-layered approaches integrating cutting-edge microbiology, biochemistry, genetics and zoology research are needed.

Highlights

  • The phylum Porifera represents the oldest extant metazoan lineage on Earth, with fossil records dating to around 580 million years ago [1,2]

  • Using cultivation-independent methods, the bacteriome of S. spinosulus and I. variabilis was found to be species-specific, deepening the observations made by means of PCR-DGGE profiling [38], whereas similar bacterial assemblages were detected in both sponge species via culturing, highlighting the bias associated with describing sponge microbiome diversity based solely on cultivation attempts

  • We know that distinct bacterial symbionts are selectively enriched within the sponge body and, eventually, vertically transmitted, and that such symbiont communities are stable along time and across geographical regions

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Summary

Introduction

The phylum Porifera (sponges) represents the oldest extant metazoan lineage on Earth, with fossil records dating to around 580 million years ago [1,2]. Eleven such ecoregions encompass 201–461 species, and are considered hot spots of marine sponge diversity [2,7] (Table 1) These animals are restricted to aquatic habitats and divided into four classes: Demospongiae, Hexactinellida, Calcarea and Homoscleromorpha, which are further distributed into 25 orders, 128 families, and 680 genera. In the light of the enormous richness of marine sponges across the globe, their contribution as the most prolific sources of marine bioactive compounds and the actual participation of their microbial symbionts in secondary metabolite biosynthesis, it is reasonable to posit that marine sponge microbiomes constitute as-yet uncharted, extremely fertile reservoirs of genetic and metabolic novelties In this context, the present review covers microbial community structure, diversity and bioactivities reported for marine sponges of the family Irciniidae (Demospongiae, Dictyoceratida), known for its wide geographical distribution (Figure 1), chemical complexity and distinct microbiota. This definition does not imply any sort of mutual benefit between hosts and symbionts

The Irciniidae Family as a Model Taxon in Sponge Microbiology Research
Microbial Diversity and Bioactivities in the Family Irciniidae
Early Microbiology Studies
Culture-Dependent Approaches
Cultivation-Independent Approaches
Method
Bioactivities
Bioactive Compounds
Archaea
Diversity
Bioactivities and Bioactive Compounds
Other Microeukaryotes
Vertical Transmission of Sponge Symbionts
Bacterial Communication and Signalling Molecules
Diseases Affecting Irciniids
Experimental Microbial Ecology
Cultivation of Irciniidae Species
Sponge Mariculture
Sponge Cell Culture
Sponge Larviculture
Findings
10. Concluding Remarks and Outlook
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