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      Microbial succession during the transition from active to inactive stages of deep-sea hydrothermal vent sulfide chimneys

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          Abstract

          Background

          Deep-sea hydrothermal vents are highly productive biodiversity hotspots in the deep ocean supported by chemosynthetic microorganisms. Prominent features of these systems are sulfide chimneys emanating high-temperature hydrothermal fluids. While several studies have investigated the microbial diversity in both active and inactive sulfide chimneys that have been extinct for up to thousands of years, little is known about chimneys that have ceased activity more recently, as well as the microbial succession occurring during the transition from active to inactive chimneys.

          Results

          Genome-resolved metagenomics was applied to an active and a recently extinct (~ 7 years) sulfide chimney from the 9–10° N hydrothermal vent field on the East Pacific Rise. Full-length 16S rRNA gene and a total of 173 high-quality metagenome assembled genomes (MAGs) were retrieved for comparative analysis. In the active chimney (L-vent), sulfide- and/or hydrogen-oxidizing Campylobacteria and Aquificae with the potential for denitrification were identified as the dominant community members and primary producers, fixing carbon through the reductive tricarboxylic acid (rTCA) cycle. In contrast, the microbiome of the recently extinct chimney (M-vent) was largely composed of heterotrophs from various bacterial phyla, including Delta-/ Beta-/ Alphaproteobacteria and Bacteroidetes. Gammaproteobacteria were identified as the main primary producers, using the oxidation of metal sulfides and/or iron oxidation coupled to nitrate reduction to fix carbon through the Calvin-Benson-Bassham (CBB) cycle. Further analysis revealed a phylogenetically distinct Nitrospirae cluster that has the potential to oxidize sulfide minerals coupled to oxygen and/or nitrite reduction, as well as for sulfate reduction, and that might serve as an indicator for the early stages of chimneys after venting has ceased.

          Conclusions

          This study sheds light on the composition, metabolic functions, and succession of microbial communities inhabiting deep-sea hydrothermal vent sulfide chimneys. Collectively, microbial succession during the life span of a chimney could be described to proceed from a “fluid-shaped” microbial community in newly formed and actively venting chimneys supported by the oxidation of reductants in the hydrothermal fluid to a “mineral-shaped” community supported by the oxidation of minerals after hydrothermal activity has ceased. Remarkably, the transition appears to occur within the first few years, after which the communities stay stable for thousands of years.

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          Most cited references97

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          Fast gapped-read alignment with Bowtie 2.

          As the rate of sequencing increases, greater throughput is demanded from read aligners. The full-text minute index is often used to make alignment very fast and memory-efficient, but the approach is ill-suited to finding longer, gapped alignments. Bowtie 2 combines the strengths of the full-text minute index with the flexibility and speed of hardware-accelerated dynamic programming algorithms to achieve a combination of high speed, sensitivity and accuracy.
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            MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability

            We report a major update of the MAFFT multiple sequence alignment program. This version has several new features, including options for adding unaligned sequences into an existing alignment, adjustment of direction in nucleotide alignment, constrained alignment and parallel processing, which were implemented after the previous major update. This report shows actual examples to explain how these features work, alone and in combination. Some examples incorrectly aligned by MAFFT are also shown to clarify its limitations. We discuss how to avoid misalignments, and our ongoing efforts to overcome such limitations.
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              RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies

              Motivation: Phylogenies are increasingly used in all fields of medical and biological research. Moreover, because of the next-generation sequencing revolution, datasets used for conducting phylogenetic analyses grow at an unprecedented pace. RAxML (Randomized Axelerated Maximum Likelihood) is a popular program for phylogenetic analyses of large datasets under maximum likelihood. Since the last RAxML paper in 2006, it has been continuously maintained and extended to accommodate the increasingly growing input datasets and to serve the needs of the user community. Results: I present some of the most notable new features and extensions of RAxML, such as a substantial extension of substitution models and supported data types, the introduction of SSE3, AVX and AVX2 vector intrinsics, techniques for reducing the memory requirements of the code and a plethora of operations for conducting post-analyses on sets of trees. In addition, an up-to-date 50-page user manual covering all new RAxML options is available. Availability and implementation: The code is available under GNU GPL at https://github.com/stamatak/standard-RAxML. Contact: alexandros.stamatakis@h-its.org Supplementary information: Supplementary data are available at Bioinformatics online.
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                Author and article information

                Contributors
                fengpingwang@sjtu.edu.cn
                zjxiao@sjtu.edu.cn
                Journal
                Microbiome
                Microbiome
                Microbiome
                BioMed Central (London )
                2049-2618
                30 June 2020
                30 June 2020
                2020
                : 8
                : 102
                Affiliations
                [1 ]GRID grid.16821.3c, ISNI 0000 0004 0368 8293, State Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology, , Shanghai Jiao Tong University, ; Shanghai, China
                [2 ]GRID grid.56466.37, ISNI 0000 0004 0504 7510, Biology Department, , Woods Hole Oceanographic Institution, ; Woods Hole, MA USA
                [3 ]GRID grid.56466.37, ISNI 0000 0004 0504 7510, Department of Marine Chemistry and Geochemistry, , Woods Hole Oceanographic Institution, ; Woods Hole, MA USA
                [4 ]GRID grid.16821.3c, ISNI 0000 0004 0368 8293, School of Oceanography, , Shanghai Jiao Tong University, ; Shanghai, China
                [5 ]Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, Guangdong China
                Author information
                http://orcid.org/0000-0002-3429-8410
                Article
                851
                10.1186/s40168-020-00851-8
                7329443
                32605604
                7c0f09f5-ee47-4684-b4c9-cf5c0c85a080
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 3 March 2020
                : 28 April 2020
                Funding
                Funded by: China Ocean Mineral Resources Research and Development Association (CN)
                Award ID: DY135-B2-12
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 91751205
                Award ID: 41530967
                Award ID: 41921006
                Award Recipient :
                Funded by: Senior User Project of RV KEXUE
                Award ID: KEXUE2019GZ06
                Award Recipient :
                Funded by: US National Science Foundation
                Award ID: OCE-1136727
                Award Recipient :
                Funded by: WHOI Investment in Science Fund
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                east pacific rise,metagenome,sulfide chimney,microbial succession,nitrospirae

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