Genomic and transcriptomic evidence of light-sensing, porphyrin biosynthesis, Calvin-Benson-Bassham cycle, and urea production in Bathyarchaeota

Abstract

Background: Bathyarchaeota, a newly proposed archaeal phylum, is considered as an important driver of the global carbon cycle. However, due to the great diversity of them, there is limited genomic information that accurately encompasses the metabolic potential of the entire archaeal phylum. Results: In the current study, nine metagenome-assembled genomes of Bathyarchaeota from four subgroups were constructed from mangrove sediments, and metatranscriptomes were obtained for evaluating their in situ transcriptional activities. Comparative analyses with reference genomes and the transcripts of functional genes posit an expanded role for Bathyarchaeota in phototrophy, autotrophy, and nitrogen and sulfur cycles, respectively. Notably, the presence of genes for rhodopsins, cobalamin biosynthesis, and the oxygen-dependent metabolic pathways in some Bathyarchaeota subgroup 6 genomes suggest a light-sensing and microoxic lifestyle within this subgroup. Conclusions: The results of this study expand our knowledge of metabolic abilities and diverse lifestyles of Bathyarchaeota, highlighting the crucial role of Bathyarchaeota in geochemical cycle.

Community, Distribution, and Ecological Roles of Estuarine Archaea

“…The abundance of Bathyarchaeota positively correlates with the concentration of total organic carbon in sediment cores in the South China Sea ( Yu et al, 2017 ) and costal mangroves ( Pan et al, 2019 , 2020 ). Enrichment experiments also confirmed that Bathyarchaeota (Bathy-8) are able to grow heterotrophically on some organic carbons, such as lignin ( Yu et al, 2018 ).…”

“…Salinity and ammonium levels are major factors influencing the distribution of Bathyarchaeota in surface sediments of the Pearl River Estuary ( Zou et al, 2020b ). On the other hand, the pH and oxygen levels, rather than salinity, are contributing factors shaping community structure of Bathyarchaeota community structure in costal mangroves and lakes ( Yoshimura et al, 2018 ; Pan et al, 2019 , 2020 ). Further, in the southern Yellow Sea and northern East China Sea, water depth, temperature, and salinity are the most influential factors determining the distribution of Bathyarchaeota in surface sediments ( Chen Y. et al, 2020 ; Liu et al, 2020 ).…”

“…Genes related to dissimilatory nitrite reduction to ammonium were also identified in these genomes, suggesting a potential capacity for nitrite reduction ( Lazar et al, 2016 ). Recently, diverse nitrogen metabolism related genes were identified in Bathyarchaeota genomes, for example the ammonium transporter ( amt ), hydroxylamine reductase ( hcp ), and nitrogenase iron protein ( nifH ) genes ( Pan et al, 2020 ). Furthermore, potential urea production pathways, including the arginase ( rocF ) and agmatinase ( speB ) pathways, were identified in some subgroups (Bathy-6, -8, and -15) in mangrove sediments ( Pan et al, 2020 ).…”

“…Recently, diverse nitrogen metabolism related genes were identified in Bathyarchaeota genomes, for example the ammonium transporter ( amt ), hydroxylamine reductase ( hcp ), and nitrogenase iron protein ( nifH ) genes ( Pan et al, 2020 ). Furthermore, potential urea production pathways, including the arginase ( rocF ) and agmatinase ( speB ) pathways, were identified in some subgroups (Bathy-6, -8, and -15) in mangrove sediments ( Pan et al, 2020 ). In addition, some Bathyarchaeota may reduce S 0 to sulfide using the hydrogenase/sulfur reductase ( hydA ), while members of Bathy-15 and -17 encode genes related to sulfate reduction and some Bathy-6 genomes harbor thiosulfate reduction genes ( Pan et al, 2020 ).…”

“…Furthermore, potential urea production pathways, including the arginase ( rocF ) and agmatinase ( speB ) pathways, were identified in some subgroups (Bathy-6, -8, and -15) in mangrove sediments ( Pan et al, 2020 ). In addition, some Bathyarchaeota may reduce S 0 to sulfide using the hydrogenase/sulfur reductase ( hydA ), while members of Bathy-15 and -17 encode genes related to sulfate reduction and some Bathy-6 genomes harbor thiosulfate reduction genes ( Pan et al, 2020 ). These findings highlight the important roles of Bathyarchaeota in benthic nitrogen and sulfur cycles, and underline their highly diverse metabolism.…”