» Articles » PMID: 39376703

Novel Thermophilic Genera Gen. Nov. and Gen. Nov. from the Deep Terrestrial Subsurface Reveal the Ecophysiological Diversity in the Class

Abstract

The class harbors a single cultivated member, the mesophilic , which was isolated from a meromictic lake. Despite numerous molecular signatures reported in various ecosystems, the ecophysiological versatility of this deeply branched lineage of remains poorly understood. The objective of this study was to use targeted cultivation, based on metagenome-assembled genomes from a deep terrestrial aquifer in Western Siberia, to isolate two new thermophilic members of the class. These isolates, described as gen. nov. sp. nov. and gen. nov. sp. nov. within the fam. nov., were capable of both anaerobic and aerobic respiration using fumarate and O, respectively, with simple sugars as electron donors. The cultivated have demonstrated fermentative growth and degradation of various polymers, including starch, maltose, maltodextrin, xylan, and chitin. The carboxydotrophic sp. nov. exhibited autotrophic growth via the Calvin-Benson-Bassham cycle, using CO, H, and formate as electron donors and O as an electron acceptor, adding metabolic flexibility to the bacterium in the nutrient-depleted "deep biosphere" and supporting the possibility of aerobic metabolism in the deep subsurface. The broad physiological potential deciphered from physiological experiments and comparative genomic data explains the widespread distribution of uncultivated members of the class in various ecosystems, where they can oxidize complex organic substrates through both aerobic and anaerobic respiration, as well as pursue a chemolithotrophic lifestyle through the oxidation of H or CO.

References
1.
Karnachuk O, Lukina A, Kadnikov V, Sherbakova V, Beletsky A, Mardanov A . Targeted isolation based on metagenome-assembled genomes reveals a phylogenetically distinct group of thermophilic spirochetes from deep biosphere. Environ Microbiol. 2020; 23(7):3585-3598. DOI: 10.1111/1462-2920.15218. View

2.
He H, Wu X, Xian H, Zhu J, Yang Y, Lv Y . An abiotic source of Archean hydrogen peroxide and oxygen that pre-dates oxygenic photosynthesis. Nat Commun. 2021; 12(1):6611. PMC: 8595356. DOI: 10.1038/s41467-021-26916-2. View

3.
Greening C, Biswas A, Carere C, Jackson C, Taylor M, Stott M . Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival. ISME J. 2015; 10(3):761-77. PMC: 4817680. DOI: 10.1038/ismej.2015.153. View

4.
Zhuravleva E, Shekhurdina S, Kotova I, Loiko N, Popova N, Kryukov E . Effects of various materials used to promote the direct interspecies electron transfer on anaerobic digestion of low-concentration swine manure. Sci Total Environ. 2022; 839:156073. DOI: 10.1016/j.scitotenv.2022.156073. View

5.
Chklovski A, Parks D, Woodcroft B, Tyson G . CheckM2: a rapid, scalable and accurate tool for assessing microbial genome quality using machine learning. Nat Methods. 2023; 20(8):1203-1212. DOI: 10.1038/s41592-023-01940-w. View