Deep-sea hydrothermal ventEpsilonproteobacteriaencode a conserved and widespread nitrate reduction pathway (Nap)

Abstract

Despite the frequent isolation of nitrate-respiring Epsilonproteobacteria from deep-sea hydrothermal vents, the genes coding for the nitrate reduction pathway in these organisms have not been investigated in depth. In this study we have shown that the gene cluster coding for the periplasmic nitrate reductase complex (nap) is highly conserved in chemolithoautotrophic, nitrate-reducing Epsilonproteobacteria from deep-sea hydrothermal vents. Furthermore, we have shown that the napA gene is expressed in pure cultures of vent Epsilonproteobacteria and it is highly conserved in microbial communities collected from deep-sea vents characterized by different temperature and redox regimes. The diversity of nitrate-reducing Epsilonproteobacteria was found to be higher in moderate temperature, diffuse flow vents than in high temperature black smokers or in low temperatures, substrate-associated communities. As NapA has a high affinity for nitrate compared with the membrane-bound enzyme, its occurrence in vent Epsilonproteobacteria may represent an adaptation of these organisms to the low nitrate concentrations typically found in vent fluids. Taken together, our findings indicate that nitrate reduction is widespread in vent Epsilonproteobacteria and provide insight on alternative energy metabolism in vent microorganisms. The occurrence of the nap cluster in vent, commensal and pathogenic Epsilonproteobacteria suggests that the ability of these bacteria to respire nitrate is important in habitats as different as the deep-sea vents and the human body.

Genome‐resolved metagenomics and metatranscriptomics reveal niche differentiation in functionally redundant microbial communities at deep‐sea hydrothermal vents

“…Moreover, these two Sulfurovum lineages have incomplete nitrate reduction pathways: while they can reduce nitrate to nitrite (encoding the nitrate reductases NR, napA, and narB), they cannot further reduce nitrite to ammonia (these MAGs lack the nitrite reductase nirA). Nitrate reduction by nap has been previously observed to be highly conserved among deep-sea hydrothermal vent Epsilonbacteraeota (Vetriani et al, 2014). Most other Sulfurovum strains had the genetic potential to use oxygen and nitrite as electron acceptors, and yet previous work has shown that the two Sulfurovum strains apparently lacking these genetic mechanisms appeared to retain a selective advantage over the other Sulfurovum strains (Anderson et al, 2017).…”

Biodiversity of Magnetotactic Bacteria in the Freshwater Lake Beloe Bordukovskoe, Russia

“…To identify certain groups of bacteria in microbial communities, one effective method is to identify genes specific to bacterial groups (41). Currently, there are many primer systems used to study bacteria that share some functional trait (42–46). For instance, genes encoding two reaction center proteins, PufLM (47, 48) and the Fenna-Matthews-Olson-protein (FmoA) (49) are used to study bacterial photosynthesis, whereas ammonia monooxygenase ( amoCAB ) genes (50) are mostly applied to investigate ammonia-oxidizing archaea.…”

Productivity, metabolism and physiology of free-living chemoautotrophic Epsilonproteobacteria

“…Despite differences in the end product, the initial step -NO 3 -reduction to NO 2 --is catalyzed by the periplasmic nitrate reductase (Nap), an enzyme complex that is evolutionarily conserved in both pathways (Vetriani et al, 2014). Although this complex conserves no energy because of its periplasmic location , its presence might permit organisms to more effectively compete in nitrate-limited environments (Potter et al, 1999).…”

“…Although this complex conserves no energy because of its periplasmic location , its presence might permit organisms to more effectively compete in nitrate-limited environments (Potter et al, 1999). As discussed above, typical vent fluid chemistry ensures electron acceptor limitation; therefore, this high-affinity nitrate respiration complex is likely an important factor underlying the success of Epsilonproteobacteria in vent environments (Vetriani et al, 2014).…”