Phylogenetic patterns in the microbial response to resource availability: amino acid incorporation in San Francisco Bay

PLoS One. 2014 Apr 21;9(4):e95842. doi: 10.1371/journal.pone.0095842. eCollection 2014.

Abstract

Aquatic microorganisms are typically identified as either oligotrophic or copiotrophic, representing trophic strategies adapted to low or high nutrient concentrations, respectively. Here, we sought to take steps towards identifying these and additional adaptations to nutrient availability with a quantitative analysis of microbial resource use in mixed communities. We incubated an estuarine microbial community with stable isotope labeled amino acids (AAs) at concentrations spanning three orders of magnitude, followed by taxon-specific quantitation of isotopic incorporation using NanoSIMS analysis of high-density microarrays. The resulting data revealed that trophic response to AA availability falls along a continuum between copiotrophy and oligotrophy, and high and low activity. To illustrate strategies along this continuum more simply, we statistically categorized microbial taxa among three trophic types, based on their incorporation responses to increasing resource concentration. The data indicated that taxa with copiotrophic-like resource use were not necessarily the most active, and taxa with oligotrophic-like resource use were not always the least active. Two of the trophic strategies were not randomly distributed throughout a 16S rDNA phylogeny, suggesting they are under selective pressure in this ecosystem and that a link exists between evolutionary relatedness and substrate affinity. The diversity of strategies to adapt to differences in resource availability highlights the need to expand our understanding of microbial interactions with organic matter in order to better predict microbial responses to a changing environment.

Publication types

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

MeSH terms

  • Amino Acids / metabolism*
  • Bays / microbiology*
  • DNA, Ribosomal / genetics
  • Ecosystem
  • Isotope Labeling / methods
  • Phylogeny*
  • San Francisco

Substances

  • Amino Acids
  • DNA, Ribosomal

Grant support

This work was supported by Lawrence Livermore National Laboratory (LLNL) Laboratory Directed Research and Development (LDRD) funding (grant # 11-ERD-066) and the Department of Energy (DOE) Office of Biological and Environmental Research (OBER) Genome Sciences Program (grant # SCW1039). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.