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Evolution of Phototrophy in the Chloroflexi Phylum Driven by Horizontal Gene Transfer

Ward, Lewis M. and Hemp, James and Shih, Patrick M. and McGlynn, Shawn E. and Fischer, Woodward W. (2018) Evolution of Phototrophy in the Chloroflexi Phylum Driven by Horizontal Gene Transfer. Frontiers in Microbiology, 9 . Art. No. 260. ISSN 1664-302X. PMCID PMC5826079. doi:10.3389/fmicb.2018.00260.

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The evolutionary mechanisms behind the extant distribution of photosynthesis is a point of substantial contention. Hypotheses range from the presence of phototrophy in the last universal common ancestor and massive gene loss in most lineages, to a later origin in Cyanobacteria followed by extensive horizontal gene transfer into the extant phototrophic clades, with intermediate scenarios that incorporate aspects of both end-members. Here, we report draft genomes of 11 Chloroflexi: the phototrophic Chloroflexia isolate Kouleothrix aurantiaca as well as 10 genome bins recovered from metagenomic sequencing of microbial mats found in Japanese hot springs. Two of these metagenome bins encode photrophic reaction centers and several of these bins form a metabolically diverse, monophyletic clade sister to the Anaerolineae class that we term Candidatus Thermofonsia. Comparisons of organismal (based on conserved ribosomal) and phototrophy (reaction center and bacteriochlorophyll synthesis) protein phylogenies throughout the Chloroflexi demonstrate that two new lineages acquired phototrophy independently via horizontal gene transfer (HGT) from different ancestral donors within the classically phototrophic Chloroflexia class. These results illustrate a complex history of phototrophy within this group, with metabolic innovation tied to HGT. These observations do not support simple hypotheses for the evolution of photosynthesis that require massive character loss from many clades; rather, HGT appears to be the defining mechanic for the distribution of phototrophy in many of the extant clades in which it appears.

Item Type:Article
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URLURL TypeDescription CentralArticle
Ward, Lewis M.0000-0002-9290-2567
Hemp, James0000-0001-7193-0553
Shih, Patrick M.0000-0002-2119-3345
McGlynn, Shawn E.0000-0002-8199-7011
Fischer, Woodward W.0000-0002-8836-3054
Additional Information:© 2018 Ward, Hemp, Shih, McGlynn and Fischer. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Received: 28 August 2017; Accepted: 01 February 2018; Published: 19 February 2018. Data Availability: Genomes described here have been deposited at GenBank and are available under the following accession numbers: K. aurantiaca (LJCR00000000), CP1_1M (PGTL00000000), CP2_20G (PGTJ00000000), CP2_2F (PGTK00000000), CP2_42A (PGTI00000000), JP1_16 (PGTG00000000), JP1_191 (PGTE00000000), JP1_20 (PGTF00000000), JP1_8 (PGTH00000000), JP3_13 (PGTM00000000), and JP3_7 (PGTN00000000). Author Contributions: LW, SM, and WF: conceived the initial study; LW and SM: collected samples; LW: processed samples and data; LW, JH, PS, SM, and WF: analyzed data; LW, JH, PS, SM, and WF: wrote the manuscript. Conflict of Interest Statement: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Acknowledgments: LW acknowledges support from NASA NESSF (#NNX16AP39H), NSF (#OISE 1639454), NSF GROW (#DGE 1144469), the Lewis and Clark Fund for Exploration and Field Research in Astrobiology, and the ELSI Origins Network. JH acknowledges support from the Agouron Institute. SM acknowledges support from MEXT KAKENHI grant-in-aid for challenging exploratory research (grant award number 15K14608). WF acknowledges the support of NASA Exobiology award (#NNX16AJ57G), the David and Lucile Packard Foundation, and a Stanford University Blaustein Fellowship. The authors would like to thank Katsumi Matsuura and the Environmental Microbiology laboratory at Tokyo Metropolitan University for laboratory support. Genomic DNA for K. aurantiaca was obtained from the Japan Collection of Microorganisms. Sequencing was performed at Seqmatic, Fremont, CA. This work was funded in part by the Center for Environmental Microbial Interactions (CEMI) at Caltech. We also thank Vera Thiel and Marcus Tank at Tokyo Metropolitan University for helpful discussions.
Group:Caltech Center for Environmental Microbial Interactions (CEMI)
Funding AgencyGrant Number
NASA Earth and Space Science FellowshipNNX16AP39H
NSF Graduate Research FellowshipDGE-1144469
Lewis and Clark Fund for Exploration and Field Research in AstrobiologyUNSPECIFIED
Agouron InstituteUNSPECIFIED
Ministry of Education, Culture, Sports, Science and Technology (MEXT)15K14608
David and Lucile Packard FoundationUNSPECIFIED
Stanford UniversityUNSPECIFIED
Caltech Center for Environmental Microbial Interactions (CEMI)UNSPECIFIED
Subject Keywords:lateral gene transfer, comparative genomics, microbial metabolism, phylogenetics, microbial diversity
PubMed Central ID:PMC5826079
Record Number:CaltechAUTHORS:20180307-130527925
Persistent URL:
Official Citation:Ward LM, Hemp J, Shih PM, McGlynn SE and Fischer WW (2018) Evolution of Phototrophy in the Chloroflexi Phylum Driven by Horizontal Gene Transfer. Front. Microbiol. 9:260. doi: 10.3389/fmicb.2018.00260
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:85180
Deposited By: Tony Diaz
Deposited On:07 Mar 2018 21:25
Last Modified:15 Nov 2021 20:26

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