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1. Sponge–Microbe Interactions on Coral Reefs: Multiple Evolutionary Solutions to a Complex Environment

   https://doi.org/10.3389/fmars.2021.705053  

   Freeman, Christopher J. ; Easson, Cole G. ; Fiore, Cara L. ; Thacker, Robert W. ( July 2021 , Frontiers in Marine Science)

   null (Ed.)

   Marine sponges have been successful in their expansion across diverse ecological niches around the globe. Pioneering work attributed this success to both a well-developed aquiferous system that allowed for efficient filter feeding on suspended organic matter and the presence of microbial symbionts that can supplement host heterotrophic feeding with photosynthate or dissolved organic carbon. We now know that sponge-microbe interactions are host-specific, highly nuanced, and provide diverse nutritional benefits to the host sponge. Despite these advances in the field, many current hypotheses pertaining to the evolution of these interactions are overly generalized; these over-simplifications limit our understanding of the evolutionary processes shaping these symbioses and how they contribute to the ecological success of sponges on modern coral reefs. To highlight the current state of knowledge in this field, we start with seminal papers and review how contemporary work using higher resolution techniques has both complemented and challenged their early hypotheses. We outline different schools of thought by discussing evidence of symbiont contribution to both host ecological divergence and convergence, nutritional specificity and plasticity, and allopatric and sympatric speciation. Based on this synthesis, we conclude that the evolutionary pressures shaping these interactions are complex, with influences from both external (nutrient limitation and competition) and internal (fitness trade-offs and evolutionary constraints) factors. We outline recent controversies pertaining to these evolutionary pressures and place our current understanding of these interactions into a broader ecological and evolutionary framework. Finally, we propose areas for future research that we believe will lead to important new developments in the field. 

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2. Chemical Ecology of Marine Sponges: New Opportunities through “-Omics”

   https://doi.org/10.1093/icb/icz014  

   Paul, Valerie J ; Freeman, Christopher J ; Agarwal, Vinayak ( April 2019 , Integrative and Comparative Biology)

   Abstract The chemical ecology and chemical defenses of sponges have been investigated for decades; consequently, sponges are among the best understood marine organisms in terms of their chemical ecology, from the level of molecules to ecosystems. Thousands of natural products have been isolated and characterized from sponges, and although relatively few of these compounds have been studied for their ecological functions, some are known to serve as chemical defenses against predators, microorganisms, fouling organisms, and other competitors. Sponges are hosts to an exceptional diversity of microorganisms, with almost 40 microbial phyla found in these associations to date. Microbial community composition and abundance are highly variable across host taxa, with a continuum from diverse assemblages of many microbial taxa to those that are dominated by a single microbial group. Microbial communities expand the nutritional repertoire of their hosts by providing access to inorganic and dissolved sources of nutrients. Not only does this continuum of microorganism–sponge associations lead to divergent nutritional characteristics in sponges, these associated microorganisms and symbionts have long been suspected, and are now known, to biosynthesize some of the natural products found in sponges. Modern “omics” tools provide ways to study these sponge–microbe associations that would have been difficult even a decade ago. Metabolomics facilitate comparisons of sponge compounds produced within and among taxa, and metagenomics and metatranscriptomics provide tools to understand the biology of host–microbe associations and the biosynthesis of ecologically relevant natural products. These combinations of ecological, microbiological, metabolomic and genomics tools, and techniques provide unprecedented opportunities to advance sponge biology and chemical ecology across many marine ecosystems. 

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3. Depth‐dependent detritus production in the sponge, Halisarca caerulea

   https://doi.org/10.1002/lno.11384  

   Lesser, Michael P. ; Mueller, Benjamin ; Pankey, M. Sabrina ; Macartney, Keir J. ; Slattery, Marc ; de Goeij, Jasper M. ( December 2019 , Limnology and Oceanography)

   Sponges are important ecological and functional components of coral reefs. Recently, a new hypothesis about the functional ecology of sponges in organic matter recycling pathways, the sponge‐loop hypothesis, in which dissolved and particulate organic matter is taken up by sponges and shunted to higher trophic levels as detritus, has been proposed and demonstrated for shallow (< 30 m) cryptic species. However, support for this hypothesis at mesophotic depths (∼ 30–150 m) is lacking. Here, we examined detritus production, a prerequisite of the sponge loop pathway, in a reciprocal transplant experiment, usingHalisarca caeruleafrom water depths of 10 and 50 m. Detritus production was significantly lower in mesophotic sponges compared to shallow samples ofH. caerulea. Additionally, detritus production rates in transplanted sponges moved in the direction of rates observed for resident conspecifics. The microbiome of these sponge populations was also significantly different between shallow and mesophotic depths, and the microbial communities of the transplanted sponges also shifted in the direction of their new depth in 10 d largely driven by changes inOxyphotobacteria,Acidimicrobiia,Nitrososphaeria,Nitrospira,Deltaproteobacteria, andDadabacteriia. This occurred in an environment where the availability of both dissolved and particulate trophic resources changed significantly across the shallow to mesophotic depth gradient where these sponge populations were found. These results suggest that changes in sponge detritus production are primarily driven by differential quality and quantity of trophic resources, as well as their utilization by the sponge host, and its microbiome, along the shallow to mesophotic depth gradient.

    

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4. Multi-Omic Profiling of Melophlus Sponges Reveals Diverse Metabolomic and Microbiome Architectures that Are Non-overlapping with Ecological Neighbors

   https://doi.org/10.3390/md18020124  

   Mohanty, Ipsita ; Podell, Sheila ; Biggs, Jason S. ; Garg, Neha ; Allen, Eric E. ; Agarwal, Vinayak ( February 2020 , Marine Drugs)

   Marine sponge holobionts, defined as filter-feeding sponge hosts together with their associated microbiomes, are prolific sources of natural products. The inventory of natural products that have been isolated from marine sponges is extensive. Here, using untargeted mass spectrometry, we demonstrate that sponges harbor a far greater diversity of low-abundance natural products that have evaded discovery. While these low-abundance natural products may not be feasible to isolate, insights into their chemical structures can be gleaned by careful curation of mass fragmentation spectra. Sponges are also some of the most complex, multi-organismal holobiont communities in the oceans. We overlay sponge metabolomes with their microbiome structures and detailed metagenomic characterization to discover candidate gene clusters that encode production of sponge-derived natural products. The multi-omic profiling strategy for sponges that we describe here enables quantitative comparison of sponge metabolomes and microbiomes to address, among other questions, the ecological relevance of sponge natural products and for the phylochemical assignment of previously undescribed sponge identities. 

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5. Presence of Bromotyrosine Alkaloids in Marine Sponges Is Independent of Metabolomic and Microbiome Architectures

   https://doi.org/10.1128/mSystems.01387-20  

   Mohanty, Ipsita ; Tapadar, Subhasish ; Moore, Samuel G. ; Biggs, Jason S. ; Freeman, Christopher J. ; Gaul, David A. ; Garg, Neha ; Agarwal, Vinayak ( April 2021 , mSystems)

   Traxler, Matthew F. (Ed.)

   ABSTRACT Marine sponge holobionts are prolific sources of natural products. One of the most geographically widespread classes of sponge-derived natural products is the bromotyrosine alkaloids. A distinguishing feature of bromotyrosine alkaloids is that they are present in phylogenetically disparate sponges. In this study, using sponge specimens collected from Guam, the Solomon Islands, the Florida Keys, and Puerto Rico, we queried whether the presence of bromotyrosine alkaloids potentiates metabolomic and microbiome conservation among geographically distant and phylogenetically different marine sponges. A multi-omic characterization of sponge holobionts revealed vastly different metabolomic and microbiome architectures among different bromotyrosine alkaloid-harboring sponges. However, we find statistically significant correlations between the microbiomes and metabolomes, signifying that the microbiome plays an important role in shaping the overall metabolome, even in low-microbial-abundance sponges. Molecules mined from the polar metabolomes of these sponges revealed conservation of biosynthetic logic between bromotyrosine alkaloids and brominated pyrrole-imidazole alkaloids, another class of marine sponge-derived natural products. In light of prior findings postulating the sponge host itself to be the biosynthetic source of bromotyrosine alkaloids, our data now set the stage for investigating the causal relationships that dictate the microbiome-metabolome interconnectedness for marine sponges in which the microbiome may not contribute to natural product biogenesis. IMPORTANCE Our work demonstrates that phylogenetically and geographically distant sponges with very different microbiomes can harbor natural product chemical classes that are united in their core chemical structures and biosynthetic logic. Furthermore, we show that independent of geographical dispersion, natural product chemistry, and microbial abundance, overall sponge metabolomes tightly correlate with their microbiomes. 

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