Abstract

Based on the Stable Ecotype Model, evolution leads to the divergence of ecologically distinct populations (e.g., with different niches and/or behaviors) of ecologically interchangeable membership. In this study, pyrosequencing was used to provide deep sequence coverage of Synechococcus psaA genes and transcripts over a large number of habitat types in the Mushroom Spring microbial mat. Putative ecological species [putative ecotypes (PEs)], which were predicted by an evolutionary simulation based on the Stable Ecotype Model (Ecotype Simulation), exhibited distinct distributions relative to temperature-defined positions in the effluent channel and vertical position in the upper 1 mm-thick mat layer. Importantly, in most cases variants predicted to belong to the same PE formed unique clusters relative to temperature and depth in the mat in canonical correspondence analysis, supporting the hypothesis that while the PEs are ecologically distinct, the members of each ecotype are ecologically homogeneous. PEs responded differently to experimental perturbations of temperature and light, but the genetic variation within each PE was maintained as the relative abundances of PEs changed, further indicating that each population responded as a set of ecologically interchangeable individuals. Compared to PEs that predominate deeper within the mat photic zone, the timing of transcript abundances for selected genes differed for PEs that predominate in microenvironments closer to upper surface of the mat with spatiotemporal differences in light and O2 concentration. All of these findings are consistent with the hypotheses that Synechococcus species in hot spring mats are sets of ecologically interchangeable individuals that are differently adapted, that these adaptations control their distributions, and that the resulting distributions constrain the activities of the species in space and time.

Highlights

  • IntroductionAcross a great diversity of microbial habitats, closely related populations have frequently shown distinct distributions along environmental gradients (West and Scanlan, 1999; Béjà et al, 2001; Ward and Cohan, 2005; Johnson et al, 2006; Walk et al, 2007; Hunt et al, 2008; Manning et al, 2008; Lau et al, 2009; Martiny et al, 2009; Miller et al, 2009; Connor et al, 2010; Denef et al, 2010; Shapiro et al, 2012; Kashtan et al, 2014)

  • Sampling This study focused on the mat community inhabiting the ∼60– 68◦C region of the major effluent channel of Mushroom Spring, an alkaline siliceous hot spring in the Lower Geyser Basin, Yellowstone National Park, WY, USA

  • Primers for the amplification of Synechococcus A/B-lineage psaA genes were designed to yield a 324 bp segment to maximize the number of single-nucleotide polymorphisms (SNPs) that could be used to differentiate PEs, and were tested for specificity to A/B -like Synechococcus sequences as described in Becraft et al (2011)

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Summary

Introduction

Across a great diversity of microbial habitats, closely related populations have frequently shown distinct distributions along environmental gradients (West and Scanlan, 1999; Béjà et al, 2001; Ward and Cohan, 2005; Johnson et al, 2006; Walk et al, 2007; Hunt et al, 2008; Manning et al, 2008; Lau et al, 2009; Martiny et al, 2009; Miller et al, 2009; Connor et al, 2010; Denef et al, 2010; Shapiro et al, 2012; Kashtan et al, 2014) These patterns have prompted the hypothesis that some microorganisms might exist as ecological species occupying distinct niches (Cohan, 1994; Ward, 1998; Ward and Cohan, 2005; Smith et al, 2006; Sikorski, 2008; Vos, 2011), as theorized in the Stable Ecotype Model of species and speciation (Cohan and Perry, 2007). Until recently, investigating the ecological interchangeability of individuals within a naturally occurring population has not been a priority of microbial speciology (Kopac et al, 2014)

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