Abstract

Genomes were obtained for three closely related strains of Synechococcus that are representative of putative ecotypes (PEs) that predominate at different depths in the 1 mm-thick, upper-green layer in the 60°C mat of Mushroom Spring, Yellowstone National Park, and exhibit different light adaptation and acclimation responses. The genomes were compared to the published genome of a previously obtained, closely related strain from a neighboring spring, and differences in both gene content and orthologous gene alleles between high-light-adapted and low-light-adapted strains were identified. Evidence of genetic differences that relate to adaptation to light intensity and/or quality, CO2uptake, nitrogen metabolism, organic carbon metabolism, and uptake of other nutrients were found between strains of the different putative ecotypes. In situ diel transcription patterns of genes, including genes unique to either low-light-adapted or high-light-adapted strains and different alleles of an orthologous photosystem gene, revealed that expression is fine-tuned to the different light environments experienced by ecotypes prevalent at various depths in the mat. This study suggests that strains of closely related PEs have different genomic adaptations that enable them to inhabit distinct ecological niches while living in close proximity within a microbial community.

Highlights

  • Thermophilic cyanobacteria of the genus Synechococcus predominate in microbial mat communities inhabiting the effluent channels of alkaline, siliceous hot springs and have been extensively studied and characterized for over 50 years (Peary and Castenholz, 1964; Brock, 1978; Ward et al, 2012)

  • Strains with these 16S rRNA genotypes were shown to have different temperature adaptations that correlated with their distribution along the effluent channel (Allewalt et al, 2006). 16S rRNA genotypes were found to differ along the vertical aspect of the mat

  • The three strains were selected because they are representative of putative ecotypes (PEs) that differ in vertical position and exhibit different adaptations to irradiance, but the low-light-adapted strains of PEs A4 and A14 were similar to each other phenotypically and were very different from the two high-light-adapted strains A1-MS and A1-OS

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Summary

Introduction

Thermophilic cyanobacteria of the genus Synechococcus predominate in microbial mat communities inhabiting the effluent channels of alkaline, siliceous hot springs and have been extensively studied and characterized for over 50 years (Peary and Castenholz, 1964; Brock, 1978; Ward et al, 2012). Genotype A′′ inhabited the highest temperatures, followed by A′, A, B′, and B as temperatures decreased with distance from the source, though some overlap of adjacent genotypes was observed Strains with these 16S rRNA genotypes were shown to have different temperature adaptations that correlated with their distribution along the effluent channel (Allewalt et al, 2006). Fluorescence microscopy, combined with estimates of oxygenic photosynthetic rates calculated using oxygen microsensor measurements in a 68◦C mat sample, revealed physiologically distinct populations in the lower and upper parts of the top green mat layer These populations were identical at the 16S rRNA locus and might have been interpreted as one genotype acclimated differently in response to lower light intensity. Surface and subsurface populations were genetically distinct at the more rapidly evolving internal transcribed spacer locus that separates the 16S and the 23S rRNA genes (Ferris et al, 2003), suggesting the possible existence of yet more closely related Synechococcus populations with different adaptations to light

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