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Title: The Expanded Diversity of Methylophilaceae from Lake Washington through Cultivation and Genomic Sequencing of Novel Ecotypes

Abstract

We describe five novel Methylophilaceae ecotypes from a single ecological niche in Lake Washington, USA, and compare them to three previously described ecotypes, in terms of their phenotype and genome sequence divergence. Two of the ecotypes appear to represent novel genera within the Methylophilaceae. Genome-based metabolic reconstruction highlights metabolic versatility of Methylophilaceae with respect to methylotrophy and nitrogen metabolism, different ecotypes possessing different combinations of primary substrate oxidation systems (MxaFI-type methanol dehydrogenase versus XoxF-type methanol dehydrogenase; methylamine dehydrogenase versus N-methylglutamate pathway) and different potentials for denitrification (assimilatory versus respiratory nitrate reduction). By comparing pairs of closely related genomes, we uncover that site-specific recombination is the main means of genomic evolution and strain divergence, including lateral transfers of genes from both closely- and distantly related taxa. The new ecotypes and the new genomes contribute significantly to our understanding of the extent of genomic and metabolic diversity among organisms of the same family inhabiting the same ecological niche. These organisms also provide novel experimental models for studying the complexity and the function of the microbial communities active in methylotrophy.

Authors:
 [1];  [1];  [1];  [1];  [1];  [2];  [3];  [2];  [1];  [1]
  1. Univ. of Washington, Seattle, WA (United States)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
OSTI Identifier:
1619062
Grant/Contract Number:  
AC02-05CH11231; SC0010556; MCB-0950183
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 9; Journal Issue: 7; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Beck, David A. C., McTaggart, Tami L., Setboonsarng, Usanisa, Vorobev, Alexey, Kalyuzhnaya, Marina G., Ivanova, Natalia, Goodwin, Lynne, Woyke, Tanja, Lidstrom, Mary E., and Chistoserdova, Ludmila. The Expanded Diversity of Methylophilaceae from Lake Washington through Cultivation and Genomic Sequencing of Novel Ecotypes. United States: N. p., 2014. Web. doi:10.1371/journal.pone.0102458.
Beck, David A. C., McTaggart, Tami L., Setboonsarng, Usanisa, Vorobev, Alexey, Kalyuzhnaya, Marina G., Ivanova, Natalia, Goodwin, Lynne, Woyke, Tanja, Lidstrom, Mary E., & Chistoserdova, Ludmila. The Expanded Diversity of Methylophilaceae from Lake Washington through Cultivation and Genomic Sequencing of Novel Ecotypes. United States. https://doi.org/10.1371/journal.pone.0102458
Beck, David A. C., McTaggart, Tami L., Setboonsarng, Usanisa, Vorobev, Alexey, Kalyuzhnaya, Marina G., Ivanova, Natalia, Goodwin, Lynne, Woyke, Tanja, Lidstrom, Mary E., and Chistoserdova, Ludmila. Thu . "The Expanded Diversity of Methylophilaceae from Lake Washington through Cultivation and Genomic Sequencing of Novel Ecotypes". United States. https://doi.org/10.1371/journal.pone.0102458. https://www.osti.gov/servlets/purl/1619062.
@article{osti_1619062,
title = {The Expanded Diversity of Methylophilaceae from Lake Washington through Cultivation and Genomic Sequencing of Novel Ecotypes},
author = {Beck, David A. C. and McTaggart, Tami L. and Setboonsarng, Usanisa and Vorobev, Alexey and Kalyuzhnaya, Marina G. and Ivanova, Natalia and Goodwin, Lynne and Woyke, Tanja and Lidstrom, Mary E. and Chistoserdova, Ludmila},
abstractNote = {We describe five novel Methylophilaceae ecotypes from a single ecological niche in Lake Washington, USA, and compare them to three previously described ecotypes, in terms of their phenotype and genome sequence divergence. Two of the ecotypes appear to represent novel genera within the Methylophilaceae. Genome-based metabolic reconstruction highlights metabolic versatility of Methylophilaceae with respect to methylotrophy and nitrogen metabolism, different ecotypes possessing different combinations of primary substrate oxidation systems (MxaFI-type methanol dehydrogenase versus XoxF-type methanol dehydrogenase; methylamine dehydrogenase versus N-methylglutamate pathway) and different potentials for denitrification (assimilatory versus respiratory nitrate reduction). By comparing pairs of closely related genomes, we uncover that site-specific recombination is the main means of genomic evolution and strain divergence, including lateral transfers of genes from both closely- and distantly related taxa. The new ecotypes and the new genomes contribute significantly to our understanding of the extent of genomic and metabolic diversity among organisms of the same family inhabiting the same ecological niche. These organisms also provide novel experimental models for studying the complexity and the function of the microbial communities active in methylotrophy.},
doi = {10.1371/journal.pone.0102458},
journal = {PLoS ONE},
number = 7,
volume = 9,
place = {United States},
year = {Thu Jul 24 00:00:00 EDT 2014},
month = {Thu Jul 24 00:00:00 EDT 2014}
}

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Cited by: 45 works
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Table 1 Table 1: Details of enrichment conditions.

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High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series Study site by phylogenetic placement of pyrosequences
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Structure of the rare archaeal biosphere and seasonal dynamics of active ecotypes in surface coastal waters
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Works referencing / citing this record:

Methylotrophs in natural habitats: current insights through metagenomics
journal, June 2015


Evolution in action: habitat transition from sediment to the pelagial leads to genome streamlining in Methylophilaceae
journal, July 2019


Lanthanide-dependent cross-feeding of methane-derived carbon is linked by microbial community interactions
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Just add lanthanides
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Evolution in action: habitat transition from sediment to the pelagial leads to genome streamlining in Methylophilaceae.
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