Genomics and the bacterial species problem

Abstract

Whether or not bacteria have species is a perennially vexatious question. Given what we now know about variation among bacterial genomes, we argue that there is no intrinsic reason why the processes driving diversification and adaptation must produce groups of individuals sufficiently coherent in their genetic and phenotypic properties to merit the designation 'species'--although sometimes they might.

Figure 1

Microdiversity and diversity in gene content. Environmental surveys, using PCR amplification and sequencing of marker genes such as 16S rRNA or more rapidly evolving protein-coding genes and intergenic spacers, often reveal microdiverse clusters of strains with closely related sequences. The diagram shows a hypothetical phylogenetic tree compiled from such sequences, with each cluster indicated by a set of circles of the same color. Such a pattern of clustering by sequence might be expected if there were process other than random divergence and extinction of lineages at play (see Figure 2), and has been attributed [11,23,24] to an ecotype speciation process (see text). In this context, a microdiverse cluster might generally be a species. Comparisons of sequenced genomes for multiple strains of many designated species, and of genome sizes from isolates of others, show, however, that gene content can vary by up to 30% among different lineages of strains, even when the 'species' marker genes are identical in sequence [25]. The different sizes of the circles represent on an exaggerated scale the diversity in genome size in closely related strains found by such studies.

Figure 2

Models of processes that promote genomic coherence. (a) The ecotype species concept and (b) the biological species concept both entail processes that lead to genomic coherence within populations and divergence (horizontal dimension) between populations. Black arrowheads indicate organisms or isolates. The crosses in (a) indicate the clones eliminated in the process, while the red arrows in (b) indicate recombination between genomes. Blue lines indicate speciation. (c) If only random lineage splitting and lineage extinction occurred, coherence would not be expected, and the designation of speciation events (dashed blue lines) would be arbitrary. In the ecotype (periodic selection) model in (a), which is applicable to organisms without significant genetic recombination, favorable mutations sweep to fixation, carrying the genome in which they first occurred along, so that diversity is reduced to zero at all loci. Accumulation of neutral mutations, prior to the next sweep, generates the sort of microdiversity illustrated in Figure 1. Gray bars are niche boundaries. In the biological species model, it is individual favorable mutations that are fixed, because recombination (indicated by red arrows) separates them from alleles at other loci in the genome in which they first occurred. Still, recombination at all loci will in time promote genomic coherence within populations and divergence between populations, because with time all alleles at all loci will be traceable to mutations that occurred within the population. The gray block indicates a barrier to recombination.

Figure 3

Lateral gene transfer and homologous recombination together can produce organisms effectively belonging to several species at once. The all-blue, all-gold and red/green circles represent genomes from three different bacterial groups that might be designated species. Each circle represents an individual genome. There is effectively no homologous recombination (arrows) between genomes or areas of different colors. LGT has, however, recently created a mosaic genome (center), with segments derived from blue, gold and red/green species (itself a mosaic). Homologous recombination can occur between a segment introduced by LGT and the corresponding region of the original donor strain. Coherence is maintained between the segments and the donor DNA, as in the biological species model. This cartoon is of course unrealistic in several respects: regions shared between species are more likely to be scattered as islands in the genome, and the number of species to which some part of any genome belongs could be much greater.