Microbial ecologists and systematists are challenged to discover the early ecological changes that drive the splitting of one bacterial population into two ecologically distinct populations. We have aimed to identify newly divergent lineages ("ecotypes") bearing the dynamic properties attributed to species, with the rationale that discovering their ecological differences would reveal the ecological dimensions of speciation. To this end, we have sampled bacteria from the Bacillus subtilis-Bacillus licheniformis clade from sites differing in solar exposure and soil texture within a Death Valley canyon. Within this clade, we hypothesized ecotype demarcations based on DNA sequence diversity, through analysis of the clade's evolutionary history by Ecotype Simulation (ES) and AdaptML. Ecotypes so demarcated were found to be significantly different in their associations with solar exposure and soil texture, suggesting that these and covarying environmental parameters are among the dimensions of ecological divergence for newly divergent Bacillus ecotypes. Fatty acid composition appeared to contribute to ecotype differences in temperature adaptation, since those ecotypes with more warm-adapting fatty acids were isolated more frequently from sites with greater solar exposure. The recognized species and subspecies of the B. subtilis-B. licheniformis clade were found to be nearly identical to the ecotypes demarcated by ES, with a few exceptions where a recognized taxon is split at most into three putative ecotypes. Nevertheless, the taxa recognized do not appear to encompass the full ecological diversity of the B. subtilis-B. licheniformis clade: ES and AdaptML identified several newly discovered clades as ecotypes that are distinct from any recognized taxon.
bClosely related bacterial genomes usually differ in gene content, suggesting that nearly every strain in nature may be ecologically unique. We have tested this hypothesis by sequencing the genomes of extremely close relatives within a recognized taxon and analyzing the genomes for evidence of ecological distinctness. We compared the genomes of four Death Valley isolates plus the laboratory strain W23, all previously classified as Bacillus subtilis subsp. spizizenii and hypothesized through multilocus analysis to be members of the same ecotype (an ecologically homogeneous population), named putative ecotype 15 (PE15). These strains showed a history of positive selection on amino acid sequences in 38 genes. Each of the strains was under a different regimen of positive selection, suggesting that each strain is ecologically unique and represents a distinct ecological speciation event. The rate of speciation appears to be much faster than can be resolved with multilocus sequencing. Each PE15 strain contained unique genes known to confer a function for bacteria. Remarkably, no unique gene conferred a metabolic system or subsystem function that was not already present in all the PE15 strains sampled. Thus, the origin of ecotypes within this clade shows no evidence of qualitative divergence in the set of resources utilized. Ecotype formation within this clade is consistent with the nanoniche model of bacterial speciation, in which ecotypes use the same set of resources but in different proportions, and genetic cohesion extends beyond a single ecotype to the set of ecotypes utilizing the same resources.
Virtually all multicellular organisms host a community of symbionts composed of mutualistic, commensal, and pathogenic microbes, i.e., their microbiome. The mechanism of selection on host-microbe assemblages remains contentious, particularly regarding whether selection acts differently on hosts and their microbial symbionts. Here, we attempt to reconcile these viewpoints using a model that describes how hosts and their microbial symbionts alter each other's niche and thereby fitness. We describe how host-microbe interactions might change the shape of the host niche and/or reproductive rates within it, which are directly related to host fitness. A host may also alter the niche of a symbiotic microbe, although this depends on the extent to which that microbe is dependent on the host for reproduction. Finally, we provide a mathematical model to test whether interactions between hosts and microbes are necessary to describe the niche of either partner. Our synthesis highlights the phenotypic effects of host-microbe interactions while respecting the unique lifestyles of each partner, and thereby provides a unified framework to describe how selection might act on a host that is associated with its microbiome.
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