Abstract
Previous analyses have shown how diversity among unicellular cyanobacteria inhabiting island-like hot springs is structured relative to physical separation and physiochemical differences among springs, especially at local to regional scales. However, these studies have been limited by the low resolution provided by the molecular markers surveyed. We analyzed large datasets obtained by high-throughput sequencing of a segment of the photosynthesis gene psaA from samples collected in hot springs from geothermal basins in Yellowstone National Park, Montana, and Oregon, all known from previous studies to contain populations of A/B′-lineage Synechococcus. The fraction of identical sequences was greater among springs separated by <50 km than among springs separated by >50 km, and springs separated by >800 km shared sequence variants only rarely. Phylogenetic analyses provided evidence for endemic lineages that could be related to geographic isolation and/or geochemical differences on regional scales. Ecotype Simulation 2 was used to predict putative ecotypes (ecologically distinct populations), and their membership, and canonical correspondence analysis was used to examine the geographical and geochemical bases for variation in their distribution. Across the range of Oregon and Yellowstone, geographical separation explained the largest percentage of the differences in distribution of ecotypes (9.5% correlated to longitude; 9.4% to latitude), with geochemical differences explaining the largest percentage of the remaining differences in distribution (7.4–9.3% correlated to magnesium, sulfate, and sulfide). Among samples within the Greater Yellowstone Ecosystem, geochemical differences significantly explained the distribution of ecotypes (6.5–9.3% correlated to magnesium, boron, sulfate, silicon dioxide, chloride, and pH). Nevertheless, differences in the abundance and membership of ecotypes in Yellowstone springs with similar chemistry suggested that allopatry may be involved even at local scales. Synechococcus populations have diverged both by physical isolation and physiochemical differences, and populations on surprisingly local scales have been evolving independently.
Highlights
Hot spring microbial mats have been used as model systems to demonstrate ecological diversification by sympatric adaptation to parameters that vary along well-established environmental gradients (Ward et al, 2012)
(i) samples were collected at different temperatures within Octopus Spring, Yellowstone National Park (YNP) and Jack’s Stream, Oregon, (ii) samples from Clearwater and Mammoth springs in YNP, and LaDuke Spring had lower pH levels than the other springs analyzed (5.2–6.9 compared to 8.1–8.8), and (iii) samples collected from Mammoth springs and LaDuke Spring had higher concentrations of calcium, magnesium, carbonate and sulfate compared to other Yellowstone springs
Allopatric and sympatric processes both appear to have played a role in the diversification of A/B′-lineage Synechococcus inhabiting the hot springs of the American Northwest
Summary
Hot spring microbial mats have been used as model systems to demonstrate ecological diversification by sympatric adaptation to parameters that vary along well-established environmental gradients (Ward et al, 2012). A progression of unicellular cyanobacterial (Synechococcus) 16S rRNA genotypes (A′′, A′, A, B′, and B, respectively) can be found along a thermal gradient in alkaline siliceous hot springs in Yellowstone National Park (YNP) (Ferris and Ward, 1997) This patterning led to the hypothesis that closely related Synechococcus populations might have different temperature adaptations and this was confirmed for isolates representative of these genotypes (Allewalt et al, 2006). Greater molecular resolution provided by a portion of the gene encoding a major photosystem I reaction center protein (psaA locus) demonstrated the existence of more closely related clades that were masked within 16S rRNA defined genotypes These clades were shown to be ecologically distinct through their associations with different light environments at different depths in the upper 1 mm in these mats (Becraft et al, 2015). The Ecotype Simulation algorithm identified sympatric ecotypes satisfying the criteria for defining ecological species: they were ecologically distinct from one another and they were each ecologically homogeneous
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