Project description:Diverse aerobic bacteria use atmospheric hydrogen (H2) and carbon monoxide (CO) as energy sources to support growth and survival. Though recently discovered, trace gas oxidation is now recognised as a globally significant process that serves as the main sink in the biogeochemical H2 cycle and sustains microbial biodiversity in oligotrophic ecosystems. While trace gas oxidation has been reported in nine phyla of bacteria, it was not known whether archaea also use atmospheric H2. Here we show that a thermoacidophilic archaeon, Acidianus brierleyi (Thermoproteota), constitutively consumes H2 and CO to sub-atmospheric levels. Oxidation occurred during both growth and survival across a wide range of temperatures (10 to 70°C). Genomic analysis demonstrated that A. brierleyi encodes a canonical carbon monoxide dehydrogenase and, unexpectedly, four distinct [NiFe]-hydrogenases from subgroups not known to mediate aerobic H2 uptake. Quantitative proteomic analyses showed that A. brierleyi differentially produced these enzymes in response to electron donor and acceptor availability. A previously unidentified group 1 [NiFe]-hydrogenase, with a unique genetic arrangement, is constitutively expressed and upregulated during stationary phase and aerobic hydrogenotrophic growth. Another archaeon, Metallosphaera sedula, was also found to oxidize atmospheric H2. These results suggest that trace gas oxidation is a common trait of aerobic archaea, which likely plays a role in their survival and niche expansion, including during dispersal through temperate environments. These findings also demonstrate that atmospheric H2 consumption is a cross-domain phenomenon, suggesting an ancient origin of this trait, and identify previously unknown microbial and enzymatic sinks of atmospheric H2 and CO.
Project description:Across the tree of life, DNA in living cells is associated with proteins that coat chromosomes, constrain their structure and influence DNA-templated processes such as transcription and replication. In bacteria and eukaryotes, HU and histones, respectively, are the principal constituents of chromatin, with few exceptions. Archaea, in contrast, have more diverse repertoires of nucleoid-associated proteins (NAPs). The evolutionary and ecological drivers behind this diversity are poorly understood. Here, we combine a systematic phylogenomic survey of known and predicted NAPs with quantitative protein abundance data to shed light on the forces governing the evolution of archaeal chromatin. Our survey identifies the Diaforarchaea as a hotbed of NAP gain and loss and we validate novel candidate NAPs in two members of this clade, Thermoplasma volcanium and Methanomassiliicoccus luminyensis, using sucrose gradient-based nucleoid enrichment coupled to quantitative mass spectrometry. Comparative analysis across a panel of 19 archaea revealed that investment in NAP production varies over two orders of magnitude, from <0.03% to >5% of total protein. Integrating genomic and ecological data, we demonstrate that growth temperature is an excellent predictor of relative NAP investment across archaea. Our results suggest that high levels of chromatinization have evolved as a mechanism toprevent uncontrolled helix opening and runaway denaturation – rather than, for example, to globally orchestrate gene expression – with implications for the origin of chromatin in both archaea and eukaryotes.