A Latitudinal Diversity Gradient in Terrestrial Bacteria of the Genus Streptomyces

Abstract

We show that Streptomyces biogeography in soils across North America is influenced by the regional diversification of microorganisms due to dispersal limitation and genetic drift.Streptomyces spp. form desiccation-resistant spores, which can be dispersed on the wind, allowing for a strong test of whether dispersal limitation governs patterns of terrestrial microbial diversity. We employed an approach that has high sensitivity for determining the effects of genetic drift. Specifically, we examined the genetic diversity and phylogeography of physiologically similar Streptomyces strains isolated from geographically distributed yet ecologically similar habitats. We found that Streptomyces beta diversity scales with geographic distance and both beta diversity and phylogenetic diversity manifest in a latitudinal diversity gradient. This pattern of Streptomyces biogeography resembles patterns seen for diverse species of plants and animals, and we therefore evaluated these data in the context of ecological and evolutionary hypotheses proposed to explain latitudinal diversity gradients. The data are consistent with the hypothesis that niche conservatism limits dispersal, and historical patterns of glaciation have limited the time for speciation in higher-latitude sites. Most notably, higher-latitude sites have lower phylogenetic diversity, higher phylogenetic clustering, and evidence of range expansion from lower latitudes. In addition, patterns of beta diversity partition with respect to the glacial history of sites. Hence, the data support the hypothesis that extant patterns of Streptomyces biogeography have been driven by historical patterns of glaciation and are the result of demographic range expansion, dispersal limitation, and regional diversification due to drift.

Importance: Biogeographic patterns provide insight into the evolutionary and ecological processes that govern biodiversity. However, the evolutionary and ecological processes that govern terrestrial microbial diversity remain poorly characterized. We evaluated the biogeography of the genus Streptomyces to show that the diversity of terrestrial bacteria is governed by many of the same processes that govern the diversity of many plant and animal species. While bacteria of the genus Streptomyces are a preeminent source of antibiotics, their evolutionary history, biogeography, and biodiversity remain poorly characterized. The observations we describe provide insight into the drivers of Streptomyces biodiversity and the processes that underlie microbial diversification in terrestrial habitats.

FIG 1

Phylogenetic (A) and taxonomic (B) dissimilarities of Streptomyces increase as a function of geographic distance between sites. The Mantel coefficient is provided along with the linear regression line.

FIG 2

Latitude correlates with the phylogenetic diversity of Streptomyces as measured by both Faith’s phylogenetic diversity (A) and the net relatedness index (B). The Pearson correlation coefficient is provided along with the linear regression line. Symbols indicate the presence (□) or absence (○) of glaciation during the late Pleistocene. Numbers rank sites by time available for colonization, as follows: 1, WI; 2, NC; 3, MS; 4, TX; 5, CA; 6, FL; 7, NY; 8, ME; 9, WA; 10, OR; 11, AK1; 12, AK2. The FL site was below sea level at the beginning of the late Pleistocene, and sites in southern Wisconsin bound the Driftless Area, which escaped glaciation and has remained above sea level since the late Paleozoic.

FIG 3

Network analysis illustrating OTU_rpoB sharing across sample sites, indicating a latitudinal gradient of beta diversity consistent with glaciation history. Sample sites (circles) are colored by history of glaciation (blue) or nonglaciation (red) during the late Pleistocene. OTUs (rectangles) are colored if both >90% of sequences were recovered from glacial (blue) or nonglacial (red) sites and the null hypothesis of random assortment was rejected (Fisher exact test, P < 0.05). The WI site was the most highly connected site in the network and has previously been proposed as a glacial refugium for certain plant species, as discussed in the text. OTUs found in only one site were excluded from the analysis.