TAXONOMY AND PHYLOGENY OF THERMOPHILIC CYANOBACTERIA INFERRED BY METAGENOMICS

Photosynthesis is pervasive in sunlit environments, and while it is a highly favorable metabolism, organisms that photosynthesize have never been found in alkaline environments above 73°C. The temperature at which thermophilic phototrophs fail to thrive is also linked to the pH: photosynthesis is constrained to temperatures < ~56°C in acidic environments. Temperature and pH also dictate the taxonomic distribution of thermophilic phototrophs. In particular cyanobacteria are the dominant oxygenic phototrophs in alkaline hot springs, while acidophilic algae are prevalent in acidic hot springs at temperatures < 56°C (1–3). Given the long evolutionary history of photosynthesis on Earth and the energetic favorability of this physiology, it is peculiar that phototrophs have not been able to overcome these temperature and pH constraints.

Here we examined the distribution of cyanobacteria across the pH-constrained upper temperature limit of oxygenic photosynthesis. We analyzed metagenomic data from hot spring samples from Yellowstone National Park with temperatures and pH ranging from 35°C to 73°C and 7.30 to 9.44, respectively. In total we recovered 30 high quality metagenome assembled genomes (MAGs). Above 60°C, and across the full range of pH sampled, early-branching cyanobacteria in the genus Leptococcus (formerly Synechococcus spp. A/B clade) (4, 5) dominate, in agreement with other studies. Three separate clades of Leptococcus were observed in these samples, each with different apparent optimal temperatures. Between 60°C and 63°C, cyanobacteria in the similarly early-branching genus Gloeomargarita (6), are also present, being most prevalent in samples at pH ~ 9.3.

The demarcation in niche space among early-branching cyanobacterial clades and other cyanobacteria raises questions about their physiological differences and evolutionary history. Further study, particularly careful genetic comparisons and experiments across a broader range of temperatures and pH are needed to better reveal the functional differences among diverged thermophilic cyanobacteria spanning different niche spaces