Functional tradeoffs underpin salinity-driven divergence in microbial community composition

PLoS One. 2014 Feb 27;9(2):e89549. doi: 10.1371/journal.pone.0089549. eCollection 2014.

Abstract

Bacterial community composition and functional potential change subtly across gradients in the surface ocean. In contrast, while there are significant phylogenetic divergences between communities from freshwater and marine habitats, the underlying mechanisms to this phylogenetic structuring yet remain unknown. We hypothesized that the functional potential of natural bacterial communities is linked to this striking divide between microbiomes. To test this hypothesis, metagenomic sequencing of microbial communities along a 1,800 km transect in the Baltic Sea area, encompassing a continuous natural salinity gradient from limnic to fully marine conditions, was explored. Multivariate statistical analyses showed that salinity is the main determinant of dramatic changes in microbial community composition, but also of large scale changes in core metabolic functions of bacteria. Strikingly, genetically and metabolically different pathways for key metabolic processes, such as respiration, biosynthesis of quinones and isoprenoids, glycolysis and osmolyte transport, were differentially abundant at high and low salinities. These shifts in functional capacities were observed at multiple taxonomic levels and within dominant bacterial phyla, while bacteria, such as SAR11, were able to adapt to the entire salinity gradient. We propose that the large differences in central metabolism required at high and low salinities dictate the striking divide between freshwater and marine microbiomes, and that the ability to inhabit different salinity regimes evolved early during bacterial phylogenetic differentiation. These findings significantly advance our understanding of microbial distributions and stress the need to incorporate salinity in future climate change models that predict increased levels of precipitation and a reduction in salinity.

Publication types

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

MeSH terms

  • Bacteria / classification*
  • Bacteria / genetics
  • Baltic States
  • Ecosystem
  • Metagenome*
  • Microbiota*
  • Phylogeny
  • RNA, Ribosomal, 16S
  • Salinity*
  • Seawater / microbiology*
  • Water Microbiology*

Substances

  • RNA, Ribosomal, 16S

Grant support

This work was supported by the Beyster Family Fund of the San Diego Foundation; Life Technologies Foundation; National Science Foundation (grant 0850256); BalticSea2020 Foundation; O. Engkvist Byggmästare Foundation; Science for Life Laboratory, Stockholm; Baltic Ecosystem Adaptive Management Program; EcoChange. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.