Microbial evolution and ecology in subzero hypersaline environments

Abstract

Microbial life, particularly prokaryotic life, is prevalent in the extreme polar settings of cryopeg and sea ice brines. Cryopegs are unfrozen layers, found in Arctic permafrost below the active layer, that are composed of relict marine sediments and their seawater-derived brines. Sea ice brines are the inhabitable liquid fraction of the contemporary ice that forms from seawater annually across the Arctic Ocean and along the Antarctic coastline. These environments each host microbial communities that contend with subzero temperatures and high salt concentrations, which present significant challenges to metabolic reaction rates and cellular stability. A major contrast between these environments is the period of exposure to stressors experienced by the inhabitants. Cryopegs remain geophysically stable under subzero hypersaline conditions over millennia while sea ice is relatively ephemeral with its brines generally lasting less than a year. The evolutionary processes that have allowed organisms to prevail in these extreme environments are deeply intertwined with the ecology of these ecosystems. This dissertation explores this entanglement by quantifying the genetic and genomic patterns of these ecosystems. Chapter 1 introduces the ideas that motivated the hypotheses driving the subsequent work aimed at understanding prokaryotic life in subzero brine environments. Chapter 2 uses environmental amplicon sequencing to explore the biodiversity of microbial communities inhabiting sea ice and cryopeg brines and assesses the observed patterns in the context of the defining environmental physics and chemistry. Chapter 3 employs cutting-edge metagenomic sequencing technology to explore evolutionary patterns of microdiversity that are prevalent in the reconstructed genomes of bacterial populations in situ, and Chapter 4 uses pangenomics to assess the evolutionary history and metabolic capabilities of Marinobacter species, the predominant bacteria inhabiting cryopeg brines. Moving through ecological scales, from communities to populations to species, this dissertation has produced the first characterization of microbial communities inhabiting cryopeg brines using environmental sequencing of 16S rRNA genes, finding them to be characterized by low levels of alpha diversity (dominated by the genus Marinobacter) and distinct by beta diversity from sea ice communities despite similarities in saline and temperature extremes. It has uncovered the importance of the mobilome (those genes involved in genome rearrangements) in the evolution of populations under constant extreme stress and quantified low levels of nucleotide diversity that are signatures of clonal expansion and selection for well-adapted genotypes in cryopeg brines. Focusing on the primary bacterial species that has flourished in cryopeg brines, it has illustrated the tremendous genetic diversity within the genus Marinobacter and identified evolutionary tactics, particularly horizontal gene transfer, and functional capabilities that have likely allowed these bacteria to prevail under constant extremes. Herein, a thorough exploration of the evolution and ecology of microbial communities inhabiting cryopeg and sea ice brines is contained, and the lessons learned from these studies is illustrated through a tome of discussions on the relevance and importance of life in these environments.