TEMPERATURE AND PH CONSTRAIN TAXONOMIC DIVERSITY AMONG THERMOPHILIC CYANOBACTERIA

Photosynthesis is pervasive in sunlit environments, and while it is a highly favorable metabolism, organisms that photosynthesize have never been found in environments above 73°C. However, the distribution of taxa in geothermal springs depends on both temperature and pH: while the highest temperature for photosynthetic growth has been observed in alkaline hot springs, this barrier is lower (~56°C) in acidic hot springs. Given the long evolutionary history of photosynthesis on Earth, and that this temperature constraint is not universally applicable to microorganisms, it is peculiar that phototrophs have not been able to overcome this barrier. Among phototrophic organisms reported at the highest temperatures, Synechococcus spp. have received the most attention, while acidophilic algae have been reported in acidic hot springs (1, 2).

Here we examined the distribution of cyanobacteria across the pH-constrained upper temperature limit of oxygenic photosynthesis. We used a combined 16S rRNA and metagenomic approach coupled to in situ microcosms and pure culture studies in hot spring samples from Yellowstone National Park with temperatures and pH ranging from 35°C to 73°C and 5.7 to 9.1, respectively. Our data reveal a stark shift in cyanobacterial taxa represented at temperature extremes across a pH gradient. Above 66°C and pH 7, early-branching cyanobacteria in the genus Leptococcus (formerly Synechococcus spp. A/B clade) (3, 4) dominate, in agreement with other studies. Cyanobacteria in the similarly early-branching genus Gloeomargarita (5), also appear to be prevalent in these alkaline high temperature samples. At lower temperatures and pH, taxonomic diversity appears to increase considerably among cyanobacteria, with a wider range of cyanobacterial taxa represented.

The observed demarcation in niche space between 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.