A Systematics for Discovering the Fundamental Units of Bacterial Diversity

Abstract

Bacterial systematists face unique challenges when trying to identify ecologically meaningful units of biological diversity. Whereas plant and animal systematists are guided by a theory-based concept of species, microbiologists have yet to agree upon a set of ecological and evolutionary properties that will serve to define a bacterial species. Advances in molecular techniques have given us a glimpse of the tremendous diversity present within the microbial world, but significant work remains to be done in order to understand the ecological and evolutionary dynamics that can account for the origin, maintenance, and distribution of that diversity. We have developed a conceptual framework that uses ecological and evolutionary theory to identify the DNA sequence clusters most likely corresponding to the fundamental units of bacterial diversity. Taking into account diverse models of bacterial evolution, we argue that bacterial systematics should seek to identify ecologically distinct groups with evidence of a history of coexistence, as based on interpretation of sequence clusters. This would establish a theory-based species unit that holds the dynamic properties broadly attributed to species outside of microbiology.

Phenotypic and genetic diversification of Pseudanabaena spp. (cyanobacteria)

“…Cluster II or the 'PCCA ecotype' occurs as a group with 99% similarity ('microdiversity cluster'), at a variety of different loci (ITS, cpcBA gene and cpcBA-IGS analysis). Previous studies indicate that such microdiversity clusters could represent important units of differentiation as ecotypes in natural populations of bacteria (Palys et al, 1997;Moore et al, 1998;Rocap et al, 2003;Konstantinidis and Tiedje, 2005;Lopez-Lopez et al, 2005;Thompson et al, 2005;Cohan, 2006;Polz et al, 2006;Cohan and Perry, 2007), and are often observed in environmental clone libraries (Field et al, 1997;Acinas et al, 2004;Morris et al, 2005;Johnson et al, 2006;Pommier et al, 2007). The microdiversity clusters identified here are correlated with morphological and ecophysiological traits such as cell length and the capacity to perform CCA (Figures 4 and 5), providing further support for the designation as an ecotype (Ahlgren and Rocap, 2006;Johnson et al, 2006;Polz et al, 2006;Ward et al, 2006).…”

“…The microdiversity clusters identified here are correlated with morphological and ecophysiological traits such as cell length and the capacity to perform CCA (Figures 4 and 5), providing further support for the designation as an ecotype (Ahlgren and Rocap, 2006;Johnson et al, 2006;Polz et al, 2006;Ward et al, 2006). Although this genetic pattern agrees with the ecotype model for bacterial species (Palys et al, 1997;Cohan, 2002;Gevers et al, 2005;Cohan and Perry, 2007), other mechanisms causing the genetic diversification of Pseudanabaena populations cannot be excluded. Indeed, the loss of substructure in the tree topology occurred when different loci were compared (e.g., ITS vs cpcBA-IGS).…”

“…Variation in the underwater light spectrum at a range of different time scales could thus have induced genetic divergence between PC-rich and CCA strains because of differences in fitness. The proposed mechanism of selective sweeps could enable such genetic diversification (Cohan, 2002(Cohan, , 2006Gevers et al, 2005;Cohan and Perry, 2007).…”

Horizontal gene transfer in evolution: facts and challenges

“…Others suggest that environmental cues may be used to define bacterial species (Cohan & Perry 2007;Ward et al 2008). Other authors (Gevers et al 2005) propose a sequential approach, using rRNA sequences to define prokaryotic genera, as well as a multi-locus sequence analysis to define species in the genera, and using different sets of genes for each genus or prokaryotic group.…”

Temporal dynamics of Prochlorococcus ecotypes in the Atlantic and Pacific oceans

“…These clades have been referred to as 'ecotypes' (Moore et al, 1998;Moore and Chisholm, 1999;Rocap et al, 2002) following the broader historical designation for genetically distinct subgroups within a species that are adapted to specific environments (Turesson, 1922;Clausen et al, 1940). They do not necessarily conform to the more recent and narrowly defined 'ecotype' concept developed by Cohan and others (Cohan, 2001;Cohan and Perry, 2007), which has become a notable model for exploring the theoretical basis for divergence among bacteria (Ward et al, 2006;Frasier et al, 2009). A more detailed discussion of the different uses of the term 'ecotype' is provided by Coleman and Chisholm, (2007).…”