Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes

Abstract

Microbes in the ocean dominate biogeochemical processes and are far more diverse than anticipated. Thus, in order to understand the ocean system, we need to delineate microbial populations with predictable ecological functions. Recent observations suggest that ocean communities comprise diverse groups of bacteria organized into genotypic (and phenotypic) clusters of closely related organisms. Although such patterns are similar to metazoan communities, the underlying mechanisms for microbial communities may differ substantially. Indeed, the potential among ocean microbes for vast population sizes, extensive migration and both homologous and illegitimate genetic recombinations, which are uncoupled from reproduction, challenges classical population models primarily developed for sexually reproducing animals. We examine possible mechanisms leading to the formation of genotypic clusters and consider alternative population genetic models for differentiation at individual loci as well as gene content at the level of whole genomes. We further suggest that ocean bacteria follow at least two different adaptive strategies, which constrain rates and bounds of evolutionary processes: the 'opportunitroph', exploiting spatially and temporally variable resources; and the passive oligotroph, efficiently using low nutrient concentrations. These ecological lifestyle differences may represent a fundamental divide with major consequences for growth and predation rates, genome evolution and population diversity, as emergent properties driving the division of labour within microbial communities.

Figure 1

Estimated temporal and spatial relationships of micro- and mesoscale features in the environment affecting the growth and productivity of marine bacteria. The region to the right and above the arrows indicates features that are captured by standard oceanographic sampling methods (modified from Dickey (1991) and Seymour (2005)).

Figure 2

Schematic of the effects of selection and HR on sequence-based phylogenetic trees. (a (i)) In the absence of selection, branch lengths reflect the coalescent process of genetic drift. (ii) After a selective sweep, branch lengths are shortened, reflecting the loss of genetic diversity. (b (i, ii)) Low rates of HR between loci result in shared genealogical histories at these loci, reflected by high correlations among phylogenies. (iii, iv) Recombination disrupts this correlation, and even after a selective event, shortened branch lengths are only observed at or genetically near the target of selection.

Figure 3

Idealized environmental distribution of sequence clusters assuming different degrees of ecological differentiation and/or stochastic processes of niche colonization. (a) Random distribution across niches with no apparent fitness differences among genotypes. (b) Clonal expansion within local niches owing to population bottlenecks or founder effects leading to apparent population structure. (c) Strong correlation with niche space indicating fitness differences. (d) Special case: microepidemics create a clonal expansion such that one genotype dominates in a localized area (bold line). Large boxes and circles denote distinct niche spaces; different symbols represent distinct populations within each niche space whereas the same symbol denotes individual strains from within the same sequence cluster.