Rusch, Douglas B

Abstract The candidate archaeal phylum ‘Aigarchaeota’ contains microorganisms from terrestrial and subsurface geothermal ecosystems. The phylogeny and metabolic potential of Aigarchaeota has been deduced from several recent single-cell amplified genomes; however, a detailed description of their metabolic potential and in situ transcriptional activity is absent. Here, we report a comprehensive metatranscriptome-based reconstruction of the in situ metabolism of Aigarchaeota in an oxic, hot spring filamentous ‘streamer’ community. Fluorescence in situ hybridization showed that these newly discovered Aigarchaeota are filamentous, which is consistent with the presence and transcription of an actin-encoding gene. Aigarchaeota filaments are intricately associated with other community members, which include both bacteria (for example, filamentous Thermocrinis spp.) and archaea. Metabolic reconstruction of genomic and metatranscriptomic data suggests that this aigarchaeon is an aerobic, chemoorganoheterotroph with autotrophic potential. A heme copper oxidase complex was identified in the environmental genome assembly and highly transcribed in situ. Potential electron donors include acetate, fatty acids, amino acids, sugars and aromatic compounds, which may originate from extracellular polymeric substances produced by other microorganisms shown to exist in close proximity and/or autochthonous dissolved organic carbon (OC). Transcripts related to genes specific to each of these potential electron donors were identified, indicating that this aigarchaeon likely utilizes several OC substrates. Characterized members of this lineage cannot synthesize heme, and other cofactors and vitamins de novo, which suggests auxotrophy. We propose the name Candidatus ‘Calditenuis aerorheumensis’ for this aigarchaeon, which describes its filamentous morphology and its primary electron acceptor, oxygen.

Abstract An uncultured member of the phylum Chlorobi, provisionally named ‘Candidatus Thermochlorobacter aerophilum’, occurs in the microbial mats of alkaline siliceous hot springs at the Yellowstone National Park. ‘Ca. T. aerophilum’ was investigated through metagenomic and metatranscriptomic approaches. ‘Ca. T. aerophilum’ is a member of a novel, family-level lineage of Chlorobi, a chlorophototroph that synthesizes type-1 reaction centers and chlorosomes similar to cultivated relatives among the green sulfur bacteria, but is otherwise very different physiologically. ‘Ca. T. aerophilum’ is proposed to be an aerobic photoheterotroph that cannot oxidize sulfur compounds, cannot fix N2, and does not fix CO2 autotrophically. Metagenomic analyses suggest that ‘Ca. T. aerophilum’ depends on other mat organisms for fixed carbon and nitrogen, several amino acids, and other important nutrients. The failure to detect bchU suggests that ‘Ca. T. aerophilum’ synthesizes bacteriochlorophyll (BChl) d, and thus it occupies a different ecological niche than other chlorosome-containing chlorophototrophs in the mat. Transcription profiling throughout a diel cycle revealed distinctive gene expression patterns. Although ‘Ca. T. aerophilum’ probably photoassimilates organic carbon sources and synthesizes most of its cell materials during the day, it mainly transcribes genes for BChl synthesis during late afternoon and early morning, and it synthesizes and assembles its photosynthetic apparatus during the night.