Strain-resolved community proteomics reveals recombining genomes of acidophilic bacteria

Abstract

Microbes comprise the majority of extant organisms, yet much remains to be learned about the nature and driving forces of microbial diversification. Our understanding of how microorganisms adapt and evolve can be advanced by genome-wide documentation of the patterns of genetic exchange, particularly if analyses target coexisting members of natural communities. Here we use community genomic data sets to identify, with strain specificity, expressed proteins from the dominant member of a genomically uncharacterized, natural, acidophilic biofilm. Proteomics results reveal a genome shaped by recombination involving chromosomal regions of tens to hundreds of kilobases long that are derived from two closely related bacterial populations. Inter-population genetic exchange was confirmed by multilocus sequence typing of isolates and of uncultivated natural consortia. The findings suggest that exchange of large blocks of gene variants is crucial for the adaptation to specific ecological niches within the very acidic, metal-rich environment. Mass-spectrometry-based discrimination of expressed protein products that differ by as little as a single amino acid enables us to distinguish the behaviour of closely related coexisting organisms. This is important, given that microorganisms grouped together as a single species may have quite distinct roles in natural systems and their interactions might be key to ecosystem optimization. Because proteomic data simultaneously convey information about genome type and activity, strain-resolved community proteomics is an important complement to cultivation-independent genomic (metagenomic) analysis of microorganisms in the natural environment.

Molecular eco-systems biology: towards an understanding of community function

“…To include this aspect of microbial interactions in global ecosystems biology, an integrated effort is needed to detect both the production of, and the response to, the plethora of small molecules that are produced by these organisms. Environmental metabolomics approaches, combined with metagenomic, meta-transcriptomic [58] and metaproteomic [59,60] data, should eventually allow the reconstruction of ecosystem-wide combined protein small-molecule networks, similar to those that have been achieved for single organisms (see Further information for a link to the STITCH chemical-protein interactions resource [61]). This approach could ultimately result in the molecular modelling of community multicellular behaviour types other than quorum sensing, such as dispersal, nutrient acquisition and biofilm formation [62].…”

A comparison of homologous recombination rates in bacteria and archaea

“…Two archaea, the thermoacidophile Sulfolobus and the halophile Halorubrum, have similar, intermediate HRR. Homologous recombination has been detected in the bacteria Thermotoga (Nesbo et al, 2006) and Leptospirillum (Lo et al, 2007) and the archaeon Ferroplasma (Tyson et al, 2004;Eppley et al, 2007), but these findings were based on non-MLST methods and so could not be included here.…”

Protein-based stable isotope probing (Protein-SIP) reveals active species within anoxic mixed cultures

“…Consequently, in recent studies, bacterial communities have been characterized by proteomic approaches (Wilmes and Bond, 2006a). The investigated environmental samples showed an intermediate complexity and were analyzed either by a separation step using 2-DE (Wilmes and Bond, 2006b;Benndorf et al, 2007) or by shotgun approaches (Ram et al, 2005;Lo et al, 2007). These studies revealed significant details about the analyzed communities, especially the different proteins involved in functional aspects.…”