Shotgun sequencing of a simple acid-mine-drainage biofilm community has recently demonstrated that, for one archaeal species population at least, individual genomes are recombinant mosaics (i.e., combinations of segments of genomes) of closely related strains. This suggests that, as in sexual organisms and contrary to current opinion, genetic exchange may be the cohesive force holding microbial species together. How, then, might microbial genomes diverge to define separate species? Since the frequency of homologous recombination decreases exponentially with genome divergence, microbial species may be naturally defined by their ability to recombine, solving a fundamental issue in biology. However, genomic mosaicism is an isolated observation in an extreme habitat that needs to be confirmed with other sympatric (geographically overlapping) microbial populations.
The problem of speciating in the face of rampant recombination is solved for sexually recombining species by geographical isolation, which allows point mutations to become fixed independently in the separated populations. However, it has long been held that geographical isolation is not possible for microorganisms because of their ability to be easily dispersed in the environment. Recent evidence indicates that some hyperthermophilic microbial species are indeed geographically isolated in hot springs. There is now a heated debate as to whether this is an exception or the rule for microorganisms. Shotgun sequencing of two geographically remote lab-scale enhanced biological phosphorus removing (EBPR) sludge communities enriched in a Rhodocyclus-like polyphosphate-accumulating organism (PAO) will address the questions of genomic mosaicism in microbial species and the related potential mechanism for speciation, geographic isolation. Strain-level polymorphisms revealed by metagenomic analysis of PAO populations will also indicate which complement of genes has been actively selected and provide insights into the evolutionary forces that have shaped the PAO populations. The work will also have considerable applied significance, since the Rhodocyclus-like PAO has only recently been identified by culture-independent methods and virtually nothing is known about the metabolic pathways this organism uses to effect EBPR.
CSP project participants: Phillip Hugenholtz (proposer, Univ. of California, Berkeley), Thomas Huber and Linda Blackall (Univ. of Queensland, Australia), Katherine McMahon (Univ. of Wisconsin-Madison), and Montgomery Slatkin (Univ. of California, Berkeley).