Novel Gloeobacterales spp. from Diverse Environments across the Globe

Abstract

Photosynthetic Cyanobacteria and their descendants are the only known organisms capable of oxygenic photosynthesis. Their metabolism permanently changed the Earth's surface and the evolutionary trajectory of life, but little is known about their evolutionary history. Genomes of the Gloeobacterales, an order of deeply divergent photosynthetic Cyanobacteria, may hold clues about the evolutionary process. However, there are only three published genomes within this order, and it is difficult to make broad inferences based on such little data. Here, I describe five species within the Gloeobacterales retrieved from publicly available databases and examine their photosynthetic gene content and the environments in which Gloeobacterales genomes and 16S rRNA gene sequences are found. The Gloeobacterales contain reduced photosystems and inhabit cold, wet-rock, and low-light environments. They are likely present in low abundances due to their low growth rate. Future searches for Gloeobacterales should target these environments, and samples should be deeply sequenced to capture the low-abundance taxa. Publicly available databases contain undescribed taxa within the Gloeobacterales. However, searching through all available data with current methods is computationally expensive. Therefore, new methods must be developed to search for these and other evolutionarily important taxa. Once identified, these novel photosynthetic Cyanobacteria will help illuminate the origin and evolution of oxygenic photosynthesis. IMPORTANCE Early branching photosynthetic Cyanobacteria such as the Gloeobacterales may provide clues into the evolutionary history of oxygenic photosynthesis, but there are few genomes or cultured taxa from this order. Five new metagenome-assembled genomes suggest that members of the Gloeobacterales all contain reduced photosystems and lack genes associated with thylakoids and circadian rhythms. Their distribution suggests that they may thrive in environments that are marginal for other species, including wet-rock and cold environments. These traits may aid in the discovery and cultivation of novel species in this clade.

Keywords: Gloeobacter; evolution; geomicrobiology; photosynthesis.

FIG 1

Maximum likelihood tree of 71 concatenated single-copy genes from genomes of “Candidatus Sericytochromatia,” “Candidatus Melainabacteria,” Gloeobacterales, and NG Cyanobacteria. New taxa are indicated in bold font. All nodes have 100% bootstrap support. Circles indicate sequences retrieved from alpine, arctic, or Antarctic environments; triangles indicate sequences from thermal springs; squares indicate sequences retrieved from rocky environments.

FIG 2

Approximate locations and environments of Gloeobacterales based on 16S rRNA gene data and retrieved genomes. Circles indicate sequences retrieved from alpine, arctic, or Antarctic environments; triangles indicate sequences from thermal springs; squares indicate sequences retrieved from rocky environments; diamonds indicate taxa recovered as endoliths in alpine environments; inverted triangles indicate sequences retrieved from other environments. The inset shows locations in the high arctic.