TY - JOUR
T1 - Groundwater Elusimicrobia are metabolically diverse compared to gut microbiome Elusimicrobia and some have a novel nitrogenase paralog
AU - Méheust, Raphaël
AU - Castelle, Cindy J.
AU - Matheus Carnevali, Paula B.
AU - Farag, Ibrahim F.
AU - He, Christine
AU - Chen, Lin Xing
AU - Amano, Yuki
AU - Hug, Laura A.
AU - Banfield, Jillian F.
N1 - Funding Information:
Acknowledgements Support was provided by grants from the Lawrence Berkeley National Laboratory’s Genomes-to-Watershed Scientific Focus Area. The U.S. Department of Energy (DOE), Office of Science, and Office of Biological and Environmental Research funded the work under contract DE-AC02-05CH11231 and the DOE carbon cycling program DOE-SC10010566. We acknowledge funding support from the Innovative Genomics Institute at Berkeley and the Chan Zuckerberg Biohub. The Ministry of Economy, Trade and Industry of Japan funded a part of the work as “The project for validating assessment methodology in geological disposal system”. Teruki Iwatsuki, Kazuki Hayashida, Toshihiro Kato, Mitsuru Kubota, Kazuya Miyakawa, and Akihito Mochizuki assisted with groundwater sampling at Mizunami and Horonobe Underground Research Laboratories, Japan Atomic Energy Agency (JAEA). C.H. acknowledges the Camille and Henry Dreyfus Foundation Postdoctoral Program in Environmental Chemistry for a Fellowship. L.A.H is supported by a Tier II Canada Research Chair.
Publisher Copyright:
© 2020, This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply.
PY - 2020/12
Y1 - 2020/12
N2 - Currently described members of Elusimicrobia, a relatively recently defined phylum, are animal-associated and rely on fermentation. However, free-living Elusimicrobia have been detected in sediments, soils and groundwater, raising questions regarding their metabolic capacities and evolutionary relationship to animal-associated species. Here, we analyzed 94 draft-quality, non-redundant genomes, including 30 newly reconstructed genomes, from diverse animal-associated and natural environments. Genomes group into 12 clades, 10 of which previously lacked reference genomes. Groundwater-associated Elusimicrobia are predicted to be capable of heterotrophic or autotrophic lifestyles, reliant on oxygen or nitrate/nitrite-dependent respiration, or a variety of organic compounds and Rhodobacter nitrogen fixation (Rnf) complex-dependent acetogenesis with hydrogen and carbon dioxide as the substrates. Genomes from two clades of groundwater-associated Elusimicrobia often encode a new group of nitrogenase paralogs that co-occur with an extensive suite of radical S-Adenosylmethionine (SAM) proteins. We identified similar genomic loci in genomes of bacteria from the Gracilibacteria phylum and the Myxococcales order and predict that the gene clusters reduce a tetrapyrrole, possibly to form a novel cofactor. The animal-associated Elusimicrobia clades nest phylogenetically within two free-living-associated clades. Thus, we propose an evolutionary trajectory in which some Elusimicrobia adapted to animal-associated lifestyles from free-living species via genome reduction.
AB - Currently described members of Elusimicrobia, a relatively recently defined phylum, are animal-associated and rely on fermentation. However, free-living Elusimicrobia have been detected in sediments, soils and groundwater, raising questions regarding their metabolic capacities and evolutionary relationship to animal-associated species. Here, we analyzed 94 draft-quality, non-redundant genomes, including 30 newly reconstructed genomes, from diverse animal-associated and natural environments. Genomes group into 12 clades, 10 of which previously lacked reference genomes. Groundwater-associated Elusimicrobia are predicted to be capable of heterotrophic or autotrophic lifestyles, reliant on oxygen or nitrate/nitrite-dependent respiration, or a variety of organic compounds and Rhodobacter nitrogen fixation (Rnf) complex-dependent acetogenesis with hydrogen and carbon dioxide as the substrates. Genomes from two clades of groundwater-associated Elusimicrobia often encode a new group of nitrogenase paralogs that co-occur with an extensive suite of radical S-Adenosylmethionine (SAM) proteins. We identified similar genomic loci in genomes of bacteria from the Gracilibacteria phylum and the Myxococcales order and predict that the gene clusters reduce a tetrapyrrole, possibly to form a novel cofactor. The animal-associated Elusimicrobia clades nest phylogenetically within two free-living-associated clades. Thus, we propose an evolutionary trajectory in which some Elusimicrobia adapted to animal-associated lifestyles from free-living species via genome reduction.
UR - http://www.scopus.com/inward/record.url?scp=85088049086&partnerID=8YFLogxK
U2 - 10.1038/s41396-020-0716-1
DO - 10.1038/s41396-020-0716-1
M3 - Article
C2 - 32681159
AN - SCOPUS:85088049086
SN - 1751-7362
VL - 14
SP - 2907
EP - 2922
JO - The ISME Journal
JF - The ISME Journal
IS - 12
ER -