The molecular dimension of microbial species: 3. Comparative genomics of Synechococcus strains with different light responses and in situ diel transcription patterns of associated putative ecotypes in the Mushroom Spring microbial mat

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.

Keywords: adaptation; comparative genomics; microbial mats; microbial species; thermophilic Synechococcus.

Figure 1

Phylogeny based on a concatenation of 460 conserved cyanobacterial proteins found in the A-lineage strains. The tree was rooted by Synechococcus sp. JA-2-3B′a(2-13) and the scale bar is equal to 0.001 amino acid substitutions/site.

Figure 2

Transcription patterns of transcripts encoding (A) PsbC in all A-lineage strains and IsiX, present in PE A4 and A14 strains, (B) ApcA/ApcB, present in all A-lineage strains, and ApcD4 LL/ApcB3 LL, present in PE A4 and A14 strains, (C) FeoA and FeoB, present in PE A4 and A14 strains, and (D) ammonium transporter genes in PE A1 (amtB1), PE A4/A14 (amtB1 LL), and duplication (amtB2 LL) in PE A4/A14. All panels show downwelling irradiance (μmol photons m⁻²s⁻¹) measured at Mushroom Spring from September 11–12, 2009.

Figure 3

rPsbA diel transcription patterns of alleles from the (i) B′ lineage, (ii) populations represented by high-light adapted strains (HL) of PE A1-OS and A1-MS, and (iii) populations represented by low-light adapted strains (LL) of PEs A4 and A14. Downwelling irradiance (μmol photons m⁻²s⁻¹) measured at Mushroom Spring on September 11–12, 2009, is also shown.