Fine-scale phylogenetic architecture of a complex bacterial community

Abstract

Although molecular data have revealed the vast scope of microbial diversity, two fundamental questions remain unanswered even for well-defined natural microbial communities: how many bacterial types co-exist, and are such types naturally organized into phylogenetically discrete units of potential ecological significance? It has been argued that without such information, the environmental function, population biology and biogeography of microorganisms cannot be rigorously explored. Here we address these questions by comprehensive sampling of two large 16S ribosomal RNA clone libraries from a coastal bacterioplankton community. We show that compensation for artefacts generated by common library construction techniques reveals fine-scale patterns of community composition. At least 516 ribotypes (unique rRNA sequences) were detected in the sample and, by statistical extrapolation, at least 1,633 co-existing ribotypes in the sampled population. More than 50% of the ribotypes fall into discrete clusters containing less than 1% sequence divergence. This pattern cannot be accounted for by interoperon variation, indicating a large predominance of closely related taxa in this community. We propose that such microdiverse clusters arise by selective sweeps and persist because competitive mechanisms are too weak to purge diversity from within them.

Low Intraspecific Diversity in a Polynucleobacter Subcluster Population Numerically Dominating Bacterioplankton of a Freshwater Pond

“…Only a few studies have revealed the microdiversity of free-living bacterial populations (1,29,42,45). The investigated PnecC population differed from these populations in a low microdiversity and a strongly uneven population structure.…”

“…We conclude that a Polynucleobacter population with an extremely low intraspecific diversity and an uneven structure numerically dominated the bacterioplankton community in the investigated habitat. This low intraspecific diversity is in strong contrast to the high intraspecific diversities found in marine bacterial populations.Microdiversity of prokaryotes, i.e., the genetic diversity within species-like (Ͼ97% similarity of 16S rRNA genes) phylogenetic groups, receives increasing attention in microbial ecology (1,5,18,19,24,28); however, the ecological significance of this diversity is still unknown. The coexistence of different bacterial genotypes belonging to the same species-like phylogenetic group is well documented for marine (1,18,19,35,45) and freshwater habitats (8,9,10,11,27,30,43).…”

“…The coexistence of different bacterial genotypes belonging to the same species-like phylogenetic group is well documented for marine (1,18,19,35,45) and freshwater habitats (8,9,10,11,27,30,43). Recently, Acinas et al (1) demonstrated by the construction and analysis of 16S rRNA clone libraries that a coastal bacterioplankton community contained a very high diversity of ribotypes, the vast majority of which fell into phylogenetically microdiverse sequence clusters (Ͻ1% divergent 16S rRNA sequences).…”

“…The monophyletic PnecC cluster is characterized by a high minimum sequence similarity of 98.5% (23) and resembles in this feature the microdiverse clusters of marine bacteria (1,42). Sequences affiliated with PnecC were previously obtained from endosymbionts of aquatic ciliates (40,44), from many freshwater habitats investigated with culture-independent methods (11,21,27,50), and from strains isolated from several freshwater habitats (23).…”

The Unique 16S rRNA Genes of Piezophiles Reflect both Phylogeny and Adaptation

“…Interestingly, the 16S sequences of all the piezophiles share high similarity with those of nonpiezophilic isolates from Antarctica. Moreover, some genera containing piezophiles (Colwellia, Psychromonas, and Moritella) appear to be largely restricted to cold waters of various depths and are underrepresented in rRNA surveys (1) and absent from environmental shotgun sequences (53) obtained from temperate waters.…”