Hu, Wenzhe

Abstract Cable bacteria are filamentous microorganisms capable of centimeter‐scale electron transport, which have great impacts on sediment biogeochemistry, especially oxygen consumption and sulfide depletion. While 16S rRNA sequences related to known cable bacteria have been identified in saline lakes, their genomic diversity, metabolic potentials, and evolution remain unknown. Eight cable bacteria genomes were retrieved from 23 sediment metagenomes across four saline lakes, representing five novel species adapted to different salinity niches. A deep‐branching Electronema species, named Electronema qinghaiense , was found preferentially in brackish to saline environments, implying an ecological and evolutionary link between marine and freshwater lineages. Based on genome analysis, the three newly named cable bacteria species are likely mixotrophic diazotrophs capable of degrading diverse complex carbohydrates, while also participating in hydrogen metabolism via various groups 3 and 4 [NiFe]‐hydrogenases. Genome streamlining and horizontal gene transfer likely drove ecophysiological differentiation among these Electrothrix and Electronema species, including an interphylum horizontal transfer of glycine/sarcosine N‐methyltransferase ( gsmt ) and sarcosine/dimethylglycine N‐methyltransferase ( sdmt ) genes into their common ancestor. Subsequent loss of these genes in some descendants led to adaptation to different salinity niches. Given the inferred ancestral physiological properties, phylogenomic analysis and the evidence that “freshwater” Electronema species experienced stronger purification selection than “saline” Electronema and “hypersaline” Electrothrix species, the evolutionary progression of cable bacteria occurred most likely in the saline‐to‐freshwater direction. Additionally, cable bacteria ecotypes adapted to specific salinity niches likely formed from selective sweeps with low homologous recombination. Collectively, these findings deepen our understanding of the ecophysiology and evolution of cable bacteria.

Summary Thermoplasmata is a widely distributed and ecologically important archaeal class in the phylum Euryarchaeota. Because few cultures and genomes are available, uncharacterized Thermoplasmata metabolisms remain unexplored. In this study, we obtained four medium‐ to high‐quality archaeal metagenome‐assembled genomes (MAGs) from the filamentous fragments of black‐odorous aquatic sediments (Foshan, Guangdong, China). Based on their 16S rRNA gene and ribosomal protein phylogenies, the four MAGs belong to the previously unnamed Thermoplasmata UBA10834 clade. We propose that this clade (five reference genomes from the Genome Taxonomy Database (GTDB) and four MAGs from this study) be considered a new order, Candidatus Gimiplasmatales. Metabolic pathway reconstructions indicated that the Ca . Gimiplasmatales MAGs can biosynthesize isoprenoids and nucleotides de novo . Additionally, some taxa have genes for formaldehyde and acetate assimilation, and the Wood–Ljungdahl CO 2 ‐fixation pathway, indicating a mixotrophic lifestyle. Sulfur reduction, hydrogen metabolism, and arsenic detoxification pathways were predicted, indicating sulfur‐, hydrogen‐, and arsenic‐transformation potentials. Comparative genomics indicated that the H 4 F Wood–Ljungdahl pathway of both Ca . Gimiplasmatales and Methanomassiliicoccales was likely obtained by the interdomain lateral gene transfer from the Firmicutes. Collectively, this study elucidates the taxonomic and potential metabolic diversity of the new order Ca . Gimiplasmatales and the evolution of this subgroup and its sister lineage Methanomassiliicoccales.