Ecological genomics of filamentous anoxygenic phototrophic bacteria inhabiting geothermal springs in Yellowstone National Park

Abstract

The filamentous anoxygenic phototrophic bacteria (FAPs) are dominant members of many phototrophic microbial mat communities in geothermal springs. In non-sulfidic springs, FAPs are known to primarily utilize photoheterotrophic metabolism, where they incorporate organic carbon sources such as glycolate or acetate, which are byproducts of cyanobacterial metabolism. Cultures of Chloroexus aurantiacus have also been shown to be capable of photoautotrophic metabolism via the 3-hydroxypropionate pathway in culture. FAPs in non-sulfidic springs have been shown to take up bicarbonate, and this behavior is stimulated by light, H 2, and H 2S. However, previously investigated mat communities contain FAPs that are more closely related to Roseiexus spp. which have not demonstrated autotrophic growth in culture. This work aimed to i ) determine whether Roseiexus spp. isolates and uncultured FAPs contain genes necessary for autotrophy, ii ) compare the community structures of FAPs in different environments, and iii ) observe patterns in gene transcription over an entire diel period, which may indicate how these organisms physiologically acclimate to changing environmental conditions. Comparisons among multiple genomes revealed that Roseiexus spp. contain genes necessary for the 3-hydroxypropionate pathway. A metagenomic investigation of the dominant constituents of the communities in Octopus Spring and Mushroom Spring resulted in the discovery of novel phototrophic organisms. Functional attributes were assigned to eight dominant ecological guilds, including three previously unknown phototrophic bacteria belonging to Kingdoms Acidobacteria, Chlorobi, and Chloroexi. Metagenomic sequencing of six communities from diverse geochemical environments revealed the presence of FAPs and other phototrophic bacteria, however there was evidence that some FAPs were unique to particular springs. Examination of transcripts produced by FAPs inhabiting Mushroom Spring indicated that genes related to phototrophy are most highly expressed at night, which presumably allows for phototrophic metabolism in the morning. Additionally, FAPs are predicted to utilize carbon and energy storage compounds such as polyglucose, wax esters, and polyhydroxyalkanoates. Based upon the transcription profiles of relevant genes, a model of their carbon and energy metabolism is proposed. Taken together, these genomic, metagenomic, and metatranscriptomic studies have advanced the understanding of FAP diversity and both the community and physiological ecology in geothermal springs.