Marine microbiome

All animals on Earth form associations with microorganisms, including protists, bacteria, archaea, fungi, and viruses. In the ocean, animal–microbial relationships were historically explored in single host–symbiont systems. However, new explorations into the diversity of marine microorganisms associating with diverse marine animal hosts is moving the field into studies that address interactions between the animal host and a more multi-member microbiome. The potential for microbiomes to influence the health, physiology, behavior, and ecology of marine animals could alter current understandings of how marine animals adapt to change, and especially the growing climate-related and anthropogenic-induced changes already impacting the ocean environment.^[1]

In the oceans, it is challenging to find

.

Background

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Deep-sea hydrothermal vent

Giant tube worms depend on symbiotic bacteria in their midgut for sustenance

The deepwater mussel Bathymodiolus childressi

depends on intracellular methanotrophic bacteria in its gills as a source of carbon

There are many outstanding questions in ecology and evolution that could be addressed by expanding the phylogenetic and ecological breadth of host-associated microbiome studies, including all possible interactions throughout the microbiome. There is strong empirical evidence and new consensus that biodiversity (i.e., the richness of species and their interactions) pervasively influences the functioning of Earth's ecosystems, including ecosystem productivity.[15]^[16] However, this research has focused almost exclusively on macroorganisms. Because microbial symbionts are integral parts of most living organisms,^[11][17] the understanding of how microbial symbionts contribute to host performance and adaptability needs broadening.^[2]

Foundations of productive ecosystems

Along with more standard examples of nutritional symbioses in animals, recent advances in

Reproduction and host development

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Extending beyond nutritional symbioses, microbial symbionts can alter the reproduction, development, and growth of their hosts. Specific bacterial strains in marine biofilms often directly control the recruitment of planktonic larvae and propagules, either by inhibiting settlement or by serving as a settlement cue.[29]^[30] For example, the settlement of zoospores from the green alga Ulva intestinalis onto the biofilms of specific bacteria is mediated by their attraction to the quorum-sensing molecule, acyl-homoserine lactone, secreted by the bacteria.^[31] Classic examples of marine host–microbe developmental dependence include the observation that algal cultures grown in isolation exhibited abnormal morphologies ^[32] and the subsequent discovery of morphogenesis-inducing compounds, such as thallusin, secreted by epiphytic bacterial symbionts.^[33] Bacteria are also known to influence the growth of marine plants, macroalgae, and phytoplankton by secreting phytohormones such as indole acetic acid and cytokinin-type hormones.^[34][35][36] In the marine choanoflagellate Salpingoeca rosetta, both multicellularity and reproduction are triggered by specific bacterial cues, offering a view into the origins of bacterial control over animal development (reviewed by Woznica and King.^[37] The benefit to the bacteria, in return, is that they receive physical space to colonize at particular points in the water column typically accessible only to planktonic microbes. Perhaps the best-studied example of intimate host–microbe interactions controlling animal development is the Hawaiian bobtail squid Euprymna scolopes.^[38] It lives in a mutualistic symbiosis with the bioluminescent bacteria Aliivibrio fischeri. The bacteria are fed a solution of sugars and amino acids by the host and, in return, provide bioluminescence for countershading and predator avoidance.^[7] This mutualism with microbes provides a selective advantage for the squid in predator–prey interactions. Another invertebrate example can be found in tubeworms, in which Hydroides elegans metamorphosis is mediated by a bacterial inducer and mitogen-activated protein kinase (MAPK) signaling in biofilms.^[39][2]

Biofouling and microbial community assembly

Some host-associated microbes produce compounds that prevent biofouling and regulate microbiome assembly and maintenance in many marine organisms, including sponges, macroalgae, and corals.^[40][41] For example, tropical corals harbor diverse bacteria in their surface mucus layer that produce quorum-sensing inhibitors and other antibacterial compounds as a defense against colonization and infection by potential microbial pathogens.^[3] Epiphytic bacteria of marine macroalgae excrete a diverse chemical arsenal capable of selectively shaping further bacterial colonization and deterring the settlement of biofouling marine invertebrates such as bryozoans.^[34][42] As in corals, these diverse, microbially secreted compounds include not only bactericidal and bacteriostatic antibiotics but also compounds like halogenated furanones, cyclic dipeptides, and acyl-homoserine lactone mimics that disrupt bacterial quorum sensing and inhibit biofilm formation.^[43] The bacteria likely are able to utilize the carbon-rich exudates from their hosts.^[44][45] For example, in the case of giant kelp, the alga emits approximately 20% of primary production as dissolved organic carbon.^[45] Whereas these prior examples illustrate how the microbiomes can protect hosts from surface colonization, a similar phenomenon has also been observed internally in the shipworm Bankia setacea, in which symbionts produce a boronated tartrolon antibiotic thought to keep the wood-digesting cecum clear of bacterial foulants.^[46] By producing antimicrobial compounds, these microbes are able to defend their niche space to prevent other organisms from crowding them out.^[2]

Biogeochemical cycling

Host-associated microbiomes also influence biogeochemical cycling within ecosystems with cascading effects on biodiversity and ecosystem processes. For example, microbial symbionts comprise up to 40% of the biomass of their sponge hosts.

These examples demonstrate the importance of microbial symbioses for the functioning of ocean ecosystems. Understanding symbioses with this same level of detail in the context of complex communities (i.e., whole microbiomes) remains ripe for exploration and, indeed, requires a more integrated framework from the fields of microbiology, evolutionary biology, community ecology, and oceanography. Individual taxa within the microbiome may help hosts withstand a wide range of environmental conditions, including those predicted under scenarios of climate change. Next, we explore two different avenues of how interdisciplinary collaborations could advance this line of research.[2]

Examples