The expanded diversity of methylophilaceae from Lake Washington through cultivation and genomic sequencing of novel ecotypes

PLoS One. 2014 Jul 24;9(7):e102458. doi: 10.1371/journal.pone.0102458. eCollection 2014.

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.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Alcohol Oxidoreductases / genetics
  • Alcohol Oxidoreductases / metabolism
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Denitrification / genetics
  • Ecotype
  • Genetic Variation
  • Genome, Bacterial*
  • Glutamates / metabolism
  • Lakes / microbiology*
  • Methylophilaceae / classification
  • Methylophilaceae / genetics
  • Methylophilaceae / metabolism*
  • Nitrogen / metabolism*
  • Oxidoreductases Acting on CH-NH Group Donors / genetics
  • Oxidoreductases Acting on CH-NH Group Donors / metabolism
  • Phylogeny*
  • Recombination, Genetic
  • Washington

Substances

  • Bacterial Proteins
  • Glutamates
  • N-methylglutamate
  • Alcohol Oxidoreductases
  • alcohol dehydrogenase (acceptor)
  • methylamine dehydrogenase
  • Oxidoreductases Acting on CH-NH Group Donors
  • Nitrogen

Grant support

This work was funded by the grants from the National Science foundation (MCB-0950183) and the Department of Energy (DE-SC0010556) and was facilitated through the use of advanced computational storage and networking infrastructure provided by the Hyak supercomputer system supported in part by the University of Washington eScience Institute. The work conducted by the U.S. Department of Energy Joint Genome Institute was supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.