Niche partitioning in the Rimicaris exoculata holobiont: the case of the first symbiotic Zetaproteobacteria

Abstract Background Free-living and symbiotic chemosynthetic microbial communities support primary production and higher trophic levels in deep-sea hydrothermal vents. The shrimp Rimicaris exoculata, which dominates animal communities along the Mid-Atlantic Ridge, houses a complex bacterial community in its enlarged cephalothorax. The dominant bacteria present are from the taxonomic groups Campylobacteria, Desulfobulbia (formerly Deltaproteobacteria), Alphaproteobacteria, Gammaproteobacteria, and some recently discovered iron oxyhydroxide-coated Zetaproteobacteria. This epibiotic consortium uses iron, sulfide, methane, and hydrogen as energy sources. Here, we generated shotgun metagenomes from Rimicaris exoculata cephalothoracic epibiotic communities to reconstruct and investigate symbiotic genomes. We collected specimens from three geochemically contrasted vent fields, TAG, Rainbow, and Snake Pit, to unravel the specificity, variability, and adaptation of Rimicaris–microbe associations. Results Our data enabled us to reconstruct 49 metagenome-assembled genomes (MAGs) from the TAG and Rainbow vent fields, including 16 with more than 90% completion and less than 5% contamination based on single copy core genes. These MAGs belonged to the dominant Campylobacteria, Desulfobulbia, Thiotrichaceae, and some novel candidate phyla radiation (CPR) lineages. In addition, most importantly, two MAGs in our collection were affiliated to Zetaproteobacteria and had no close relatives (average nucleotide identity ANI < 77% with the closest relative Ghiorsea bivora isolated from TAG, and 88% with each other), suggesting potential novel species. Genes for Calvin-Benson Bassham (CBB) carbon fixation, iron, and sulfur oxidation, as well as nitrate reduction, occurred in both MAGs. However, genes for hydrogen oxidation and multicopper oxidases occurred in one MAG only, suggesting shared and specific potential functions for these two novel Zetaproteobacteria symbiotic lineages. Overall, we observed highly similar symbionts co-existing in a single shrimp at both the basaltic TAG and ultramafic Rainbow vent sites. Nevertheless, further examination of the seeming functional redundancy among these epibionts revealed important differences. Conclusion These data highlight microniche partitioning in the Rimicaris holobiont and support recent studies showing that functional diversity enables multiple symbiont strains to coexist in animals colonizing hydrothermal vents.

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Niche Partitioning in the Rimicaris Exoculata Holobiont: The Case of the First Symbiotic Zetaproteobacteria

10.21203/rs.3.rs-136571/v1 ◽

2020 ◽

Author(s):

Marie-Anne Cambon-Bonavita ◽

Johanne Aubé ◽

Valérie Cueff-Gauchard ◽

Julie Reveillaud

Keyword(s):

Hydrothermal Vents ◽

Carbon Fixation ◽

Iron Sulfide ◽

Hydrogen Oxidation ◽

Niche Partitioning ◽

Sulfur Oxidation ◽

Single Copy ◽

Rimicaris Exoculata ◽

Invertebrate Animals ◽

Close Relatives

Abstract Background Mutualistic symbioses between invertebrate animals and chemosynthetic bacteria are the basis of life in hydrothermal vent ecosystems. The shrimp Rimicaris exoculata , which dominates animal communities along the Mid-Atlantic Ridge, houses a complex bacterial community in its enlarged cephalothorax, including the dominant Campylobacteria , Desulfobulbia (formerly Deltaproteobacteria ), Alpha proteobacteria , Gammaproteobacteria and some recently discovered iron oxyhydroxide-coated Zetaproteobacteria . This epibiotic consortium uses iron, sulfide, methane, and hydrogen as energy sources. Here, we generated shotgun metagenomes from Rimicaris exoculata cephalothoracic epibiotic communities to reconstruct and investigate symbiotic genomes. We collected specimens in three geochemically contrasted vent fields, TAG, Rainbow, and Snake Pit, to unravel the specificity, variability, and adaptation of Rimicaris –microbe associations. Results Our data enabled us to reconstruct 49 metagenome-assembled genomes (MAGs) from the TAG and Rainbow vent fields, including 16 with more than 90% completion and less than 5% contamination based on single copy core genes. These MAGs belonged to the dominant Campylobacteria , Desulfobulbia , Thiotrichaceae as well as some novel candidate phyla radiation (CPR) lineages. In addition, most importantly, two MAGs in our collection were affiliated to Zetaproteobacteria and had no close relatives (average nucleotide identity ANI < 77% with the closest relative Ghiorsea bivora isolated from TAG, and 88% with each other), suggesting potential novel species. Genes for Calvin-Benson Bassham (CBB) carbon fixation, iron, and sulfur oxidation, as well as nitrate reduction, occurred in both MAGs. However, genes for hydrogen oxidation and multicopper oxidases occurred in one MAG only, suggesting shared and specific potential functions for these two novel Zetaproteobacteria symbiotic lineages. Overall, we observed highly similar symbionts co-existing in a single shrimp at both the basaltic TAG and ultramafic Rainbow vent sites. Nevertheless, further examination of the seeming functional redundancy among these epibionts revealed important differences. Conclusion These data highlight microniche partitioning in the Rimicaris holobiont and support recent studies showing that functional diversity enables multiple symbiont strains to coexist in animals colonizing hydrothermal vents.

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Niche Partitioning in the Rimicaris Exoculata Holobiont: The Case of the First Symbiotic Zetaproteobacteria

10.21203/rs.3.rs-33129/v1 ◽

2020 ◽

Author(s):

Marie-Anne Cambon-Bonavita ◽

Johanne Aubé ◽

Valérie Cueff-Gauchard ◽

Julie Reveillaud

Keyword(s):

Hydrothermal Vents ◽

Carbon Fixation ◽

Iron Sulfide ◽

Hydrogen Oxidation ◽

Niche Partitioning ◽

Extraction Procedure ◽

Sulfur Oxidation ◽

Rimicaris Exoculata ◽

Invertebrate Animals ◽

Close Relatives

Abstract BackgroundMutualistic symbioses between invertebrate animals and chemosynthetic bacteria are at the basis of Life in hydrothermal vent ecosystems. The shrimp Rimicaris exoculata, which dominates animal fauna along the Mid Atlantic Ridge, houses in its cephalothorax a complex bacterial community including Campylobacteria, Gamma- Delta- and some recently discovered iron oxyhydroxides-coated Zetaproteobacteria. This epibiotic consortium uses iron, sulfide, methane and hydrogen as energy sources. Here, we used a DNA extraction procedure adapted to recalcitrant embedded bacteria and generated shotgun metagenomes from Rimicaris exoculata cephalothoracic epibiotic community. We aimed reconstructing symbiotic genomes from specimen collected in three geochemically contrasted vent fields, TAG, Rainbow and Snake Pit to unravel the specificity, variability and adaptation of host-microbes associations.ResultsUsing these data we were able to reconstruct 49 high quality metagenome-assembled genomes (MAGs) from TAG and Rainbow vents fields. Most critically, two MAGs in our collection were affiliated to Zetaproteobacteria and had no close relatives (ANI < 77% from the closest relative Ghiorsea bivora isolated from TAG and <88% between each other), suggesting potential novel species. Genes for CBB carbon fixation, iron and sulfur oxidation, as well as nitrate reduction, occurred in both MAGs. However, genes for hydrogen oxidation and quorum sensing as well as multicopper oxidases occurred in one MAG only, suggesting shared and specific potential functions for these two novel Zetaproteobacteria symbiotic lineages. Overall, we observed highly similar symbionts that co-exist in a single shrimp at both basaltic TAG and ultramafic Rainbow vent sites. Nevertheless, further insights into the seemingly functional redundancy between those epibionts revealed important differences. ConclusionThese data highlight microniche partitioning in the Rimicaris holobiont and confirm recent works that show functional diversity enables multiple symbiont strains to coexist in animals from hydrothermal vents.

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Host–Endosymbiont Genome Integration in a Deep-Sea Chemosymbiotic Clam

Molecular Biology and Evolution ◽

10.1093/molbev/msaa241 ◽

2020 ◽

Cited By ~ 1

Author(s):

Jack Chi-Ho Ip ◽

Ting Xu ◽

Jin Sun ◽

Runsheng Li ◽

Chong Chen ◽

...

Keyword(s):

Deep Sea ◽

Hydrothermal Vents ◽

Carbon Fixation ◽

Sulfur Oxidation ◽

Gene Families ◽

Cold Seeps ◽

Cellular Processes ◽

Metabolic Integration ◽

Metabolite Exchange ◽

Chemosynthetic Bacteria

Abstract Endosymbiosis with chemosynthetic bacteria has enabled many deep-sea invertebrates to thrive at hydrothermal vents and cold seeps, but most previous studies on this mutualism have focused on the bacteria only. Vesicomyid clams dominate global deep-sea chemosynthesis-based ecosystems. They differ from most deep-sea symbiotic animals in passing their symbionts from parent to offspring, enabling intricate coevolution between the host and the symbiont. Here, we sequenced the genomes of the clam Archivesica marissinica (Bivalvia: Vesicomyidae) and its bacterial symbiont to understand the genomic/metabolic integration behind this symbiosis. At 1.52 Gb, the clam genome encodes 28 genes horizontally transferred from bacteria, a large number of pseudogenes and transposable elements whose massive expansion corresponded to the timing of the rise and subsequent divergence of symbiont-bearing vesicomyids. The genome exhibits gene family expansion in cellular processes that likely facilitate chemoautotrophy, including gas delivery to support energy and carbon production, metabolite exchange with the symbiont, and regulation of the bacteriocyte population. Contraction in cellulase genes is likely adaptive to the shift from phytoplankton-derived to bacteria-based food. It also shows contraction in bacterial recognition gene families, indicative of suppressed immune response to the endosymbiont. The gammaproteobacterium endosymbiont has a reduced genome of 1.03 Mb but retains complete pathways for sulfur oxidation, carbon fixation, and biosynthesis of 20 common amino acids, indicating the host’s high dependence on the symbiont for nutrition. Overall, the host–symbiont genomes show not only tight metabolic complementarity but also distinct signatures of coevolution allowing the vesicomyids to thrive in chemosynthesis-based ecosystems.

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Mobula kuhlii cleaning station identified at an inshore reef in southern Mozambique

10.7287/peerj.preprints.1724 ◽

2016 ◽

Author(s):

Calum JG Murie ◽

Andrea D Marshall

Keyword(s):

Niche Partitioning ◽

Labroides Dimidiatus ◽

Cleaning Station ◽

Inshore Reef ◽

Close Relatives ◽

Distinct Body

Cleaning interactions between the short fin devil ray, Mobula kuhlii, and the blue streaked cleaner wrasse, Labroides dimidiatus, were observed at two sites on a single reef in southern Mozambique. Cleaning interactions were filmed and described, with the number and location of interactions recorded and subsequently binned into six distinct body patches. Cleaners preferentially foraged within certain ray body patches, and this was found to vary between the two sites, possibly signifying that variations in a habitats composition can influence cleaning. Mobula kuhlii were not found to clean sympatrically with their close relatives in the Manta genus, implying their cleaning requires a distinct habitat or that niche partitioning is required to stem competition for host cleaner fishes attention. In total, 15 individuals were observed interacting with cleaners, and they never arrived alone, suggesting they may travel to cleaning areas in an aggregative manner.

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Microbial dark carbon fixation fueled by nitrate enrichment

10.1101/2021.08.24.457596 ◽

2021 ◽

Author(s):

Joseph H. Vineis ◽

Ashley N. Bulseco ◽

Jennifer L. Bowen

Keyword(s):

Microbial Communities ◽

Marine Sediments ◽

Salt Marshes ◽

Carbon Fixation ◽

Niche Partitioning ◽

Coastal Marine Sediments ◽

Functional Relationships ◽

Coastal Marine ◽

Dark Carbon Fixation ◽

The Impact

Anthropogenic nitrate amendment to coastal marine sediments can increase rates of heterotrophic mineralization and autotrophic dark carbon fixation (DCF). DCF may be favored in sediments where organic matter is biologically unavailable, leading to a microbial community supported by chemoautotrophy. Niche partitioning among DCF communities and adaptations for nitrate metabolism in coastal marine sediments remain poorly characterized, especially within salt marshes. We used genome-resolved metagenomics, phylogenetics, and comparative genomics to characterize the potential niche space, phylogenetic relationships, and adaptations important to microbial communities within nitrate enriched sediment. We found that nitrate enrichment of sediment from discrete depths between 0-25 cm supported both heterotrophs and chemoautotrophs that use sulfur oxidizing denitrification to drive the Calvin-Benson-Bassham (CBB) or reductive TCA (rTCA) DCF pathways. Phylogenetic reconstruction indicated that the nitrate enriched community represented a small fraction of the phylogenetic diversity contained in coastal marine environmental genomes, while pangenomics revealed close evolutionary and functional relationships with DCF microbes in other oligotrophic environments. These results indicate that DCF can support coastal marine microbial communities and should be carefully considered when estimating the impact of nitrate on carbon cycling in these critical habitats.

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Cycles, Compartments, and Polymerization

Assembling Life ◽

10.1093/oso/9780190646387.003.0014 ◽

2019 ◽

Author(s):

David W. Deamer

Keyword(s):

Genetic Information ◽

Hydrothermal Vents ◽

Carbon Fixation ◽

Energy Sources ◽

Hydrothermal Conditions ◽

Biologically Relevant ◽

Cellular Life ◽

Primitive Metabolism ◽

Chain Lengths ◽

Design Experiments

The two quotes in the epigraph, in juxtaposition, always make me smile, and I tried to keep them in mind while writing this chapter. The first eight chapters of this book have the effect of eliminating the impossible by investigating the facts to which Twain is referring. Perhaps he would consider them trifling, but I doubt that Twain ever performed an experiment to test an idea. Every working scientist knows that science is not just a set of facts but is also a set of questions. The best way to begin answering a question is to pose a hypothesis and that hypothesis begins as a conjecture. Only when we have a hypothesis, can we design experiments to test it, and if we are lucky, the results of those experiments lead us a little closer to the truth. This chapter summarizes facts that lead to an alternative scenario for life’s origin in freshwater hydrothermal conditions rather than a marine origin in saltwater hydrothermal vents. As stated in the introduction to this book, when assumptions are part of the story they will be made explicit so that the logic that arises from them will be clear. What follows in this overview is a list of ten prerequisites we assume are necessary for cellular life to begin, followed by eight assumptions underlying the scenario to be presented here. Prerequisite conditions for life to begin: Dilute solutions of potential reactants are available, together with a process by which they can be sufficiently concentrated to react. Energy sources available in the environment can drive reactions such as carbon fixation, primitive metabolism, and polymerization. Products of reactions accumulate within the site rather than dispersing into the bulk phase environment. Amphiphiles assemble into membranous compartments over the range of temperatures, salt concentrations, and pH values related to each site. Biologically relevant polymers are synthesized with chain lengths sufficient to act as catalysts or incorporate genetic information. A plausible physical mechanism can produce encapsulated polymers as protocells then subject them to combinatorial selection. Organic solutes in aqueous solutions become biochemical solutes within protocells and then substrates supporting a primitive metabolism.

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Food sources, behaviour, and distribution of hydrothermal vent shrimps at the Mid-Atlantic Ridge

Journal of the Marine Biological Association of the United Kingdom ◽

10.1017/s0025315400002186 ◽

2000 ◽

Vol 80 (3) ◽

pp. 485-499 ◽

Cited By ~ 80

Author(s):

A.V. Gebruk ◽

E.C. Southward ◽

H. Kennedy ◽

A.J. Southward

Keyword(s):

Hydrothermal Vents ◽

Food Sources ◽

Larval Stages ◽

Rimicaris Exoculata ◽

Tube Worms ◽

The Pacific ◽

Mid Atlantic Ridge ◽

Menez Gwen ◽

Juvenile Shrimp ◽

Supporting Structures

Five species of bresilioid shrimp were investigated at seven hydrothermal sites on the Mid-Atlantic Ridge: Menez Gwen, Lucky Strike, Rainbow, Broken Spur, TAG, Snake Pit and Logatchev. Samples were prepared for analysis of stable isotopes, elemental composition and lipids. Shrimp behaviour was observed from the submersible ‘Alvin’ and in the laboratory aboard RV ‘Atlantis’. The distribution and zonation of the shrimp species was recorded. Juvenile shrimp of all species arrive at the vents carrying reserves of photosynthetic origin, built-up in the pelagic larval stages. These reserves are used while the shrimp metamorphose to the adult form and, in Rimicaris exoculata and Chorocaris chacei, while they develop epibiotic bacteria supporting structures, the modified mouthparts and the inside of the carapace. The main food of adult R. exoculata is filamentous bacteria that grow on these structures. The intermediate sizes of C. chacei also feed on such bacteria, but the final stage gets some food by scavenging or predation. Mirocaris species scavenge diverse sources; they are not trophically dependent on either R. exoculata or mussels. Adults of Alvinocaris markensis are predators of other vent animals, including R. exoculata. The dense swarms of R. exoculata, with their exosymbionts, can be compared to endosymbiont-containing animals such as Bathymodiolus and the vestimentiferan tube-worms of the Pacific vents. Such associations, whether endo- or ectosymbiotic, may be necessary for the development of flourishing communities at hydrothermal vents.

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Organ of Bellonci and Sinus Gland in Three Decapods from Atlantic Hydrothermal Vents: Rimicaris Exoculata, Chorocaris Chacei, and Segonzacia Mesatlantica

Journal of Crustacean Biology ◽

10.2307/1549315 ◽

1998 ◽

Vol 18 (2) ◽

pp. 213-223 ◽

Cited By ~ 5

Author(s):

Mireille Charmantier-Daures ◽

Michel Segonzac

Keyword(s):

Hydrothermal Vents ◽

Sinus Gland ◽

Rimicaris Exoculata

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Nitrite Reductase Genes (nirK andnirS) as Functional Markers To Investigate Diversity of Denitrifying Bacteria in Pacific Northwest Marine Sediment Communities

Applied and Environmental Microbiology ◽

10.1128/aem.66.5.2096-2104.2000 ◽

2000 ◽

Vol 66 (5) ◽

pp. 2096-2104 ◽

Cited By ~ 338

Author(s):

Gesche Braker ◽

Jizhong Zhou ◽

Liyou Wu ◽

Allan H. Devol ◽

James M. Tiedje

Keyword(s):

Pacific Northwest ◽

Gene Tree ◽

Puget Sound ◽

Pseudomonas Stutzeri ◽

Single Copy ◽

Denitrifying Bacteria ◽

Small Samples ◽

Functional Markers ◽

Sediment Samples ◽

Close Relatives

ABSTRACT Genetic heterogeneity of denitrifying bacteria in sediment samples from Puget Sound and two sites on the Washington continental margin was studied by PCR approaches amplifying nirK andnirS genes. These structurally different but functionally equivalent single-copy genes coding for nitrite reductases, a key enzyme of the denitrification process, were used as a molecular marker for denitrifying bacteria. nirS sequences could be amplified from samples of both sampling sites, whereas nirKsequences were detected only in samples from the Washington margin. To assess the underlying nir gene structure, PCR products of both genes were cloned and screened by restriction fragment length polymorphism (RFLP). Rarefraction analysis revealed a high level of diversity especially for nirS clones from Puget Sound and a slightly lower level of diversity for nirK andnirS clones from the Washington margin. One group dominated within nirK clones, but no dominance and only a few redundant clones were seen between sediment samples fornirS clones in both habitats. Hybridization and sequencing confirmed that all but one of the 228 putative nirS clones were nirS with levels of nucleotide identities as low as 45.3%. Phylogenetic analysis grouped nirS clones into three distinct subclusters within the nirS gene tree which corresponded to the two habitats from which they were obtained. These sequences had little relationship to any strain with knownnirS sequences or to isolates (mostly close relatives ofPseudomonas stutzeri) from the Washington margin sediment samples. nirK clones were more closely related to each other than were the nirS clones, with 78.6% and higher nucleotide identities; clones showing only weak hybridization signals were not related to known nirK sequences. AllnirK clones were also grouped into a distinct cluster which could not be placed with any strain with known nirKsequences. These findings show a very high diversity of nirsequences within small samples and that these novel nirclusters, some very divergent from known sequences, are not known in cultivated denitrifiers.

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