In situ ecophysiology of Aigarchaeota from an oxic, hot-spring filamentous ‘streamer’ community

Tuesday, 16 December 2014
Jacob Beam1, Zackary Jay1, Susannah G Tringe2, Tijana Glavina del Rio2, Douglas Rusch3, Markus Schmid4, Michael Wagner4 and William Inskeep1, (1)Montana State University, Bozeman, MT, United States, (2)DOE Joint Genome Institute, Walnut Creek, CA, United States, (3)Indiana University Bloomington, The Center for Genomics and Bioinformatics, Bloomington, IN, United States, (4)University of Vienna, Divison of Microbial Ecology, Vienna, Austria
The candidate phylum Aigarchaeota contains thermophilic archaea from terrestrial, subsurface, and marine geothermal ecosystems. The phylogeny and metabolic potential of Aigarchaeota has been deduced from several recent single-cell amplified genomes; however, an accurate description of their metabolism, potential ecological interactions, and role in biogeochemical cycling is lacking. Here we report possible ecological interactions and the in situ metabolism of an uncultivated lineage of Aigarchaeota from an oxic, terrestrial hot-spring filamentous ‘streamer’ community (Octopus Spring, pH = 8; T = 78 – 84 °C, Yellowstone National Park, Wyoming, USA). Fluorescence in situ hybridization (FISH) was combined with detailed genomic and transcriptomic reconstruction to elucidate the ecophysiological role of Aigarchaeota in these streamer communities. This novel population of Aigarchaeota are filamentous (~500 nm diameter by ~10-30 μm length), which is consistent with the morphology predicted by the presence and transcription of a single actin-encoding gene. Aigarchaeota filaments are intricately associated with other community members, which include both thermophilic bacteria and archaea. Metabolic reconstruction suggests that this aigarchaeon is an aerobic, chemoorganotroph. A single heme copper oxidase complex was identified in de novo genome assemblies, and was highly transcribed in environmental samples. Potential electron donors include acetate, fatty acids, sugars, peptides, and aromatic compounds. Transcripts related to genes specific to each of these potential electron donors were identified, indicating that this population of Aigarchaeota likely utilizes a broad range of reduced carbon substrates. Potential electron donors for this population may include extracellular polymeric substances produced by other microorganisms in close proximity. Flagellum genes were also highly transcribed, which suggests a potential mechanism for motility and/or cell-cell attachment. This study provides the first evidence for the in situ metabolism and possible ecological interactions of a novel lineage of Aigarchaeota that are globally distributed in oxic hot-spring ecosystems.