Abstract
Microbial populations inhabiting a natural hypersaline lake ecosystem in Lake Tyrrell, Victoria, Australia, have been characterized using deep metagenomic sampling, iterative de novo assembly, and multidimensional phylogenetic binning. Composite genomes representing habitat-specific microbial populations were reconstructed for eleven different archaea and one bacterium, comprising between 0.6 and 14.1% of the planktonic community. Eight of the eleven archaeal genomes were from microbial species without previously cultured representatives. These new genomes provide habitat-specific reference sequences enabling detailed, lineage-specific compartmentalization of predicted functional capabilities and cellular properties associated with both dominant and less abundant community members, including organisms previously known only by their 16S rRNA sequences. Together, these data provide a comprehensive, culture-independent genomic blueprint for ecosystem-wide analysis of protein functions, population structure, and lifestyles of co-existing, co-evolving microbial groups within the same natural habitat. The “assembly-driven” community genomic approach demonstrated in this study advances our ability to push beyond single gene investigations, and promotes genome-scale reconstructions as a tangible goal in the quest to define the metabolic, ecological, and evolutionary dynamics that underpin environmental microbial diversity.
Highlights
Microbial diversity studies based on 16S rRNA gene amplification have identified large numbers of uncultured, uncharacterized organisms whose metabolic capabilities, lifestyle strategies, and ecosystem contributions remain largely unknown
The extreme hypersaline habitat of Lake Tyrrell, Australia has recently been used to demonstrate the utility of de novo metagenomic assembly for characterizing organisms previously known only by their 16S rRNA gene sequences, including representatives of a globally distributed new class of Archaea, the Nanohaloarchaea [13,14]. We extend this previous work, combining cell size-fractionated sample collection, deep metagenomic sequencing, multidimensional phylogenetic binning, and iterative de novo assembly to reconstruct ten additional population genomes
Because the percent G+C content of individual microorganisms tends to be relatively uniform when averaged over long stretches of DNA, consolidated scaffold peaks in a length-weighted G+C histogram like Figure 1 are useful in surveying diversity of dominant microbial populations within a mixed community
Summary
Microbial diversity studies based on 16S rRNA gene amplification have identified large numbers of uncultured, uncharacterized organisms whose metabolic capabilities, lifestyle strategies, and ecosystem contributions remain largely unknown. The subset of cultured microbial species from any particular habitat often fails to include even some of the most abundant members of the community. Efforts to bring these unknown organisms into laboratory culture are confounded by our limited understanding of the metabolic specializations of environmental microorganisms, the interdependencies of intra-/inter-species interactions, and the physicochemical conditions that promote or diminish microbial survival and population structure in natural environments. Environmental sampling of predicted metabolic functions as a simple ‘‘bag of genes’’ via metagenomic readbased analysis cannot fully capture the genetic and metabolic potential of individual populations, and may overlook the significance of community-wide processes involving cooperative interactions between multiple species [7,8,9]
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