TY - JOUR
T1 - Ecology and molecular targets of hypermutation in the global microbiome
AU - Roux, Simon
AU - Paul, Blair G.
AU - Bagby, Sarah C.
AU - Nayfach, Stephen
AU - Allen, Michelle A.
AU - Attwood, Graeme
AU - Cavicchioli, Ricardo
AU - Chistoserdova, Ludmila
AU - Gruninger, Robert J.
AU - Hallam, Steven J.
AU - Hernandez, Maria E.
AU - Hess, Matthias
AU - Liu, Wen Tso
AU - McAllister, Tim A.
AU - O’Malley, Michelle A.
AU - Peng, Xuefeng
AU - Rich, Virginia I.
AU - Saleska, Scott R.
AU - Eloe-Fadrosh, Emiley A.
N1 - Funding Information:
We thank Sean Crowe, Laura A. Hug, Kelly C. Wrighton, Stuart E. Denman, Gonzalo Martinez-Fernandez, Christopher S. McSweeney, and Katherine D. McMahon for providing detailed information on unpublished metagenomes. The work conducted by the U.S. Department of Energy Joint Genome Institute is supported by the Office of Science of the U.S. Department of Energy under contract no. DE-AC02-05CH11231. This research used resources of the National Energy Research Scientific Computing Center (NERSC), a U.S. Department of Energy Office of Science User Facility operated under Contract No. DE-AC02-05CH11231. B.G.P. was supported by the Marine Biological Laboratory, by the National Science Foundation’s XSEDE computing resource (award DEB170007), and through a Challenge Grant from the California NanoSystems Institute at the University of California Santa Barbara. S.C.B. was partially supported by the U.S. Department of Energy under award DE-SC0020173. M.A.O. acknowledges funding support from the National Science Foundation (NSF) (MCB-1553721), the Camille Dreyfus Teacher-Scholar Awards Program, and the California NanoSystems Institute (CNSI) Challenge Grant Program, supported by the University of California, Santa Barbara and the University of California, Office of the President. This work was part of the DOE Joint BioEnergy Institute (http://www.jbei.org) supported by the Office of Biological and Environmental Research of the DOE Office of Science through contract DE-AC02–05CH11231 between Lawrence Berkeley National Laboratory and the DOE. R. C. was supported by the Australian Research Council (DP150100244) and the Australian Antarctic Science program (project 4031). The work in the Hallam Lab was performed under the auspices of the US Department of Energy (DOE) Joint Genome Institute, an Office of Science User Facility, supported by the Office of Science of the U.S. Department of Energy under Contract DE-AC02-05CH11231 through the Community Science Program (CSP), the G. Unger Vetlesen and Ambrose Monell Foundations, the Natural Sciences and Engineering Research Council of Canada, Genome British Columbia, Genome Canada, and Compute Canada and the Canada Foundation for Innovation through grants awarded to S.J.H., R.J.G. and T.A.M. acknowledge funding from Agriculture and Agri-Food Canada, the Beef Cattle Research Council and the Alberta Beef Producers. V.I.R. and S.R.S. acknowledge support for the IsoGenie Project (samples and metadata from Stordalen Mire, Sweden) by the Genomic Science Program of the United States Department of Energy Office of Biological and Environmental Research (DESC0004632, DE-SC0010580, DE-SC0016440), and acknowledge the IsoGenie Project Team. S.R., S.C.B., V.I.R., S.R.S. and E.A.E.-F. acknowledge support from the EMERGE Institute (NSF #2022070). Sequencing of the Stordalen Mire samples used herein was performed under BER Support Science Proposal 503530, conducted by the U.S. Department of Energy Joint Genome Institute, which is supported as described above. This manuscript has been authored by authors at Lawrence Berkeley National Laboratory under Contract No. DE-AC02-05CH11231 with the U.S. Department of Energy. The U.S. Government retains, and the publisher, by accepting the article for publication, acknowledges, that the U.S. Government retains a non-exclusive, paid-up, irrevocable, worldwide license to publish or reproduce the published form of this manuscript, or allow others to do so, for U.S. Government purposes.
Publisher Copyright:
© 2021, The Author(s).
PY - 2021/12/1
Y1 - 2021/12/1
N2 - Changes in the sequence of an organism’s genome, i.e., mutations, are the raw material of evolution. The frequency and location of mutations can be constrained by specific molecular mechanisms, such as diversity-generating retroelements (DGRs). DGRs have been characterized from cultivated bacteria and bacteriophages, and perform error-prone reverse transcription leading to mutations being introduced in specific target genes. DGR loci were also identified in several metagenomes, but the ecological roles and evolutionary drivers of these DGRs remain poorly understood. Here, we analyze a dataset of >30,000 DGRs from public metagenomes, establish six major lineages of DGRs including three primarily encoded by phages and seemingly used to diversify host attachment proteins, and demonstrate that DGRs are broadly active and responsible for >10% of all amino acid changes in some organisms. Overall, these results highlight the constraints under which DGRs evolve, and elucidate several distinct roles these elements play in natural communities.
AB - Changes in the sequence of an organism’s genome, i.e., mutations, are the raw material of evolution. The frequency and location of mutations can be constrained by specific molecular mechanisms, such as diversity-generating retroelements (DGRs). DGRs have been characterized from cultivated bacteria and bacteriophages, and perform error-prone reverse transcription leading to mutations being introduced in specific target genes. DGR loci were also identified in several metagenomes, but the ecological roles and evolutionary drivers of these DGRs remain poorly understood. Here, we analyze a dataset of >30,000 DGRs from public metagenomes, establish six major lineages of DGRs including three primarily encoded by phages and seemingly used to diversify host attachment proteins, and demonstrate that DGRs are broadly active and responsible for >10% of all amino acid changes in some organisms. Overall, these results highlight the constraints under which DGRs evolve, and elucidate several distinct roles these elements play in natural communities.
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U2 - 10.1038/s41467-021-23402-7
DO - 10.1038/s41467-021-23402-7
M3 - Article
C2 - 34031405
AN - SCOPUS:85106571392
SN - 2041-1723
VL - 12
JO - Nature communications
JF - Nature communications
IS - 1
M1 - 3076
ER -