Cross-tolerance between osmotic and freeze-thaw stress in microbial assemblages from temperate lakes

Authors

  • Sandra L. Wilson,

    1. Department of Biology, Queen's University, Kingston, ON, Canada
    Current affiliation:
    1. Department of Biological Sciences, University of Calgary, Calgary, AB, Canada
    Search for more papers by this author
  • Corey Frazer,

    1. Department of Biology, Queen's University, Kingston, ON, Canada
    Current affiliation:
    1. Department of Biomedical and Molecular Sciences, Queen's University, Kingston, ON, Canada
    Search for more papers by this author
  • Brian F. Cumming,

    1. Department of Biology, Queen's University, Kingston, ON, Canada
    2. School of Environmental Studies, Queen's University, Kingston, ON, Canada
    Search for more papers by this author
  • Paulo A.S. Nuin,

    1. Department of Pathology and Molecular Medicine, Queen's University, Kingston, ON, Canada
    Search for more papers by this author
  • Virginia K. Walker

    Corresponding author
    1. School of Environmental Studies, Queen's University, Kingston, ON, Canada
    • Department of Biology, Queen's University, Kingston, ON, Canada
    Search for more papers by this author

Correspondence: Virginia K. Walker, Department of Biology, Queen's University, Kingston, ON K7L 3N6, Canada. Tel.: (613) 533 6123; fax: (613) 533 6617; e-mail: walkervk@queensu.ca

Abstract

Osmotic stress can accompany increases in solute concentrations because of freezing or high-salt environments. Consequently, microorganisms from environments with a high-osmotic potential may exhibit cross-tolerance to freeze stress. To test this hypothesis, enrichments derived from the sediment and water of temperate lakes with a range of salt concentrations were subjected to multiple freeze-thaw cycles. Surviving isolates were identified and metagenomes were sampled prior to and following selection. Enrichments from alkali lakes were typically the most freeze-thaw resistant with only 100-fold losses in cell viability, and those from freshwater lakes were most susceptible, with cell numbers reduced at least 100 000-fold. Metagenomic analysis suggested that selection reduced assemblage diversity more in freshwater samples than in those from saline lakes. Survivors included known psychro-, halo- and alkali-tolerant bacteria. Characterization of freeze-thaw-resistant isolates from brine and alkali lakes showed that few isolates had ice-associating activities such as antifreeze or ice nucleation properties. However, all brine- and alkali-derived isolates had high intracellular levels of osmolytes and/or appeared more likely to form biofilms. Conversely, these phenotypes were infrequent amongst the freshwater-derived isolates. These observations are consistent with microbial cross-tolerance between osmotic and freeze-thaw stresses.

Ancillary