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      Integrative taxonomy revisits the ontogeny and trophic niches of Rimicaris vent shrimps

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          Abstract

          Among hydrothermal vent species, Rimicaris exoculata is one of the most emblematic, hosting abundant and diverse ectosymbioses that provide most of its nutrition. Rimicaris exoculata co-occurs in dense aggregates with the much less abundant Rimicaris chacei in many Mid-Atlantic Ridge vent fields. This second shrimp also houses ectosymbiotic microorganisms but has a mixotrophic diet. Recent observations have suggested potential misidentifications between these species at their juvenile stages, which could have led to misinterpretations of their early-life ecology. Here, we confirm erroneous identification of the earliest stages and propose a new set of morphological characters unambiguously identifying juveniles of each species. On the basis of this reassessment, combined use of C, N and S stable isotope ratios reveals distinct ontogenic trophic niche shifts in both species, from photosynthesis-based nutrition before settlement, towards a chemosynthetic diet afterwards. Furthermore, isotopic compositions in the earliest juvenile stages suggest differences in larval histories. Each species thus exhibits specific early-life strategies that would, without our re-examination, have been interpreted as ontogenetic variations. Overall, our results provide a good illustration of the identification issues persisting in deep-sea ecosystems and the importance of integrative taxonomy in providing an accurate view of fundamental aspects of the biology and ecology of species inhabiting these environments.

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          Deep, diverse and definitely different: unique attributes of the world's largest ecosystem

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            Beyond the Calvin cycle: autotrophic carbon fixation in the ocean.

            Organisms capable of autotrophic metabolism assimilate inorganic carbon into organic carbon. They form an integral part of ecosystems by making an otherwise unavailable form of carbon available to other organisms, a central component of the global carbon cycle. For many years, the doctrine prevailed that the Calvin-Benson-Bassham (CBB) cycle is the only biochemical autotrophic CO2 fixation pathway of significance in the ocean. However, ecological, biochemical, and genomic studies carried out over the last decade have not only elucidated new pathways but also shown that autotrophic carbon fixation via pathways other than the CBB cycle can be significant. This has ramifications for our understanding of the carbon cycle and energy flow in the ocean. Here, we review the recent discoveries in the field of autotrophic carbon fixation, including the biochemistry and evolution of the different pathways, as well as their ecological relevance in various oceanic ecosystems.
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              Comparative Genomic Analysis of the Class Epsilonproteobacteria and Proposed Reclassification to Epsilonbacteraeota (phyl. nov.)

              The Epsilonproteobacteria is the fifth validly described class of the phylum Proteobacteria, known primarily for clinical relevance and for chemolithotrophy in various terrestrial and marine environments, including deep-sea hydrothermal vents. As 16S rRNA gene repositories have expanded and protein marker analysis become more common, the phylogenetic placement of this class has become less certain. A number of recent analyses of the bacterial tree of life using both 16S rRNA and concatenated marker gene analyses have failed to recover the Epsilonproteobacteria as monophyletic with all other classes of Proteobacteria. In order to address this issue, we investigated the phylogenetic placement of this class in the bacterial domain using 16S and 23S rRNA genes, as well as 120 single-copy marker proteins. Single- and concatenated-marker trees were created using a data set of 4,170 bacterial representatives, including 98 Epsilonproteobacteria. Phylogenies were inferred under a variety of tree building methods, with sequential jackknifing of outgroup phyla to ensure robustness of phylogenetic affiliations under differing combinations of bacterial genomes. Based on the assessment of nearly 300 phylogenetic tree topologies, we conclude that the continued inclusion of Epsilonproteobacteria within the Proteobacteria is not warranted, and that this group should be reassigned to a novel phylum for which we propose the name Epsilonbacteraeota (phyl. nov.). We further recommend the reclassification of the order Desulfurellales (Deltaproteobacteria) to a novel class within this phylum and a number of subordinate changes to ensure consistency with the genome-based phylogeny. Phylogenomic analysis of 658 genomes belonging to the newly proposed Epsilonbacteraeota suggests that the ancestor of this phylum was an autotrophic, motile, thermophilic chemolithotroph that likely assimilated nitrogen from ammonium taken up from the environment or generated from environmental nitrate and nitrite by employing a variety of functional redox modules. The emergence of chemoorganoheterotrophic lifestyles in several Epsilonbacteraeota families is the result of multiple independent losses of various ancestral chemolithoautotrophic pathways. Our proposed reclassification of this group resolves an important anomaly in bacterial systematics and ensures that the taxonomy of Proteobacteria remains robust, specifically as genome-based taxonomies become more common.
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                Author and article information

                Journal
                R Soc Open Sci
                R Soc Open Sci
                RSOS
                royopensci
                Royal Society Open Science
                The Royal Society
                2054-5703
                July 2020
                8 July 2020
                8 July 2020
                : 7
                : 7
                : 200837
                Affiliations
                [1 ]Ifremer, Univ Brest, CNRS, Laboratoire de Microbiologie des Environnements Extrêmes, UMR 6197 , F-29280 Plouzané, France
                [2 ]Ifremer, Centre Brest, Laboratoire Environnement Profond (REM/EEP/LEP), ZI de la pointe du Diable , F-29280 Plouzané, France
                [3 ]Institut de Systématique, Évolution, Biodiversité (ISYEB), Muséum national d'Histoire naturelle, CNRS, Sorbonne Université, EPHE , case postale 53, 57 rue Cuvier, F-75231 Paris cedex 05, France
                Author notes
                Author for correspondence: Florence Pradillon e-mail: florence.pradillon@ 123456ifremer.fr

                Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.5046714.

                Author information
                http://orcid.org/0000-0001-5454-1775
                http://orcid.org/0000-0003-0988-7050
                http://orcid.org/0000-0002-4076-0472
                http://orcid.org/0000-0002-6473-6290
                Article
                rsos200837
                10.1098/rsos.200837
                7428246
                32874664
                afab4cda-ac6c-4f9c-959c-5045ff53cdb4
                © 2020 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 19 May 2020
                : 17 June 2020
                Funding
                Funded by: Région Bretagne, http://dx.doi.org/10.13039/501100011697;
                Award ID: ARED
                Funded by: Institut Français de Recherche pour l'Exploitation de la Mer, http://dx.doi.org/10.13039/100009111;
                Award ID: REMIMA
                Categories
                1001
                60
                183
                129
                Organismal and Evolutionary Biology
                Research Article
                Custom metadata
                July, 2020

                hydrothermal vents,stable isotopes,taxonomy,crustaceans,life history,trophic shift

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