Microbiomes and Obligate Symbiosis of Deep-Sea Animals

Abstract

Microbial communities associated with deep-sea animals are critical to the establishment of novel biological communities in unusual environments. Over the past few decades, rapid exploration of the deep sea has enabled the discovery of novel microbial communities, some of which form symbiotic relationships with animal hosts. Symbiosis in the deep sea changes host physiology, behavior, ecology, and evolution over time and space. Symbiont diversity within a host is often aligned with diverse metabolic pathways that broaden the environmental niche for the animal host. In this review, we focus on microbiomes and obligate symbionts found in different deep-sea habitats and how they facilitate survival of the organisms that live in these environments. In addition, we discuss factors that govern microbiome diversity, host specificity, and biogeography in the deep sea. Finally, we highlight the current limitations of microbiome research and draw a road map for future directions to advance our knowledge of microbiomes in the deep sea. Expected final online publication date for the Annual Review of Animal Biosciences, Volume 10 is February 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Insights into symbiotic interactions from metatranscriptome analysis of deep‐sea mussel Gigantidas platifrons under long‐term laboratory maintenance

“…Establishing a symbiotic relationship with chemosynthetic bacteria is the most remarkable achievement of animals living deep below the ocean surface because it enables them to colonize the hydrothermal vent and methane seep ecosystems worldwide (Dubilier et al, 2008; Osman & Weinnig, 2022). In these symbiotic associations, the survival of host animals is highly reliant on the energy and nutrition provided by symbiotic bacteria through the oxidation of reduced compounds (e.g., reduced sulfur compounds, methane, and hydrogen) in the environment (Dubilier et al, 2008; Petersen et al, 2011; Sogin et al, 2021).…”

Interactions among deep-sea mussels and their epibiotic and endosymbiotic chemoautotrophic bacteria: Insights from multi-omics analysis

“…Nevertheless, the release of abundant reducing chemicals, such as hydrogen sulfide, methane, and hydrogen, from the seafloor of these habitats promotes bacterial chemosynthesis to support thriving communities of invertebrates such as giant tubeworms, clams, mussels, and snails ( Sen et al, 2018 ; Van Dover, 2000 ). Symbiosis between deep-sea invertebrates and chemosynthetic bacteria has allowed the colonization of these deep-sea habitats despite very limited input of organic matter from photosynthesis in surface waters ( Childress et al, 1986 ; Dubilier et al, 2008 ; Osman & Weinnig, 2022 ). The formation of symbiosis requires substantial structural changes in the host, such as the replacement of the digestive tract by trophosomes (bacterial-hosting organ in the trunk) in giant tubeworms and degeneration of the digestive tract in bathymodioline mussels and vesicomyid clams ( Osman & Weinnig, 2022 ).…”

“…Symbiosis between deep-sea invertebrates and chemosynthetic bacteria has allowed the colonization of these deep-sea habitats despite very limited input of organic matter from photosynthesis in surface waters ( Childress et al, 1986 ; Dubilier et al, 2008 ; Osman & Weinnig, 2022 ). The formation of symbiosis requires substantial structural changes in the host, such as the replacement of the digestive tract by trophosomes (bacterial-hosting organ in the trunk) in giant tubeworms and degeneration of the digestive tract in bathymodioline mussels and vesicomyid clams ( Osman & Weinnig, 2022 ).…”

“…Research over the past four decades has revealed the diversity of chemosynthetic holobionts with respect to habitats, symbiont locations, and host and symbiont taxa ( Ansorge et al, 2019 ; Dubilier et al, 2008 ; Lim et al, 2019 ; Osman & Weinnig, 2022 ). Among holobionts, bathymodioline mussels have been studied extensively ( Duperron et al, 2008 ; Laming et al, 2018 ; Lin et al, 2021 ; Roeselers & Newton, 2012 ), with a focus on endosymbiotic Gammaproteobacteria that live inside host bacteriocytes – epithelial cells that contain symbionts.…”

Capacity of deep‐sea corals to obtain nutrition from cold seeps aligned with microbiome reorganization

“…Other animals associate with chemosynthetic microbes (Fisher et al, 2007 ) that convert toxic to non‐toxic substances and fix carbon (Laso‐Pérez et al, 2019 ; Niemann et al, 2013 ; Sogin et al, 2020 ). Most cold seep fauna (e.g., siboglind tubeworm, bathymodiolus mussels) have chemosymbiotic microbes and/or upregulate expression of genes related to the innate immune system, heavy metal detoxification, and metabolic pathways involving sulfide when toxic chemicals are present in the environment (Cheng et al, 2019 ; Osman & Weinnig, 2022 ; Sogin et al, 2020 ; Wong et al, 2015 ).…”