Expanded Diversity and Metabolic Versatility of Marine Nitrite-Oxidizing Bacteria Revealed by Cultivation- and Genomics-Based Approaches

Abstract

Nitrite-oxidizing bacteria (NOB) are ubiquitous and abundant microorganisms that play key roles in global nitrogen and carbon biogeochemical cycling. Despite recent advances in understanding NOB physiology and taxonomy, there are currently very few cultured NOB or representative NOB genome sequences from marine environments. In this study, we employed enrichment culturing and genomic approaches in order to shed light on the phylogeny and metabolic capacity of marine NOB. We successfully enriched two marine NOB (designated MSP and DJ) and obtained a high-quality metagenome-assembled genome (MAG) from each organism. The maximum nitrite oxidation rates of the MSP and DJ enrichment cultures were 13.8 (0.1 mM nitrite as optimum) and 30.0 μM (0.3 mM nitrite) nitrite per day, respectively. Each enrichment culture exhibited different tolerance to varying nitrite and salt concentrations. Based on phylogenomic position and overall genome relatedness indices, both NOB MAGs were proposed as novel taxa within the Nitrospinota and Nitrospirota phyla. Functional predictions indicated that both NOB MAGs shared many highly conserve metabolic features with other NOB. Both NOB MAGs encoded proteins for hydrogen and organic compound metabolism and defense mechanisms for oxidative stress. Additionally, these organisms may have the genetic potential to produce cobalamin (an essential enzyme cofactor that is limiting in many environments) and thus may play an important role in recycling cobalamin in marine sediment. Overall, this study appreciably expands our understanding of the Nitrospinota and Nitrospirota phyla, and suggests that these NOB may play important biogeochemical roles in marine habitats. Importance Nitrification is a key process in the biogeochemical and global nitrogen cycle. Nitrite-oxidizing bacteria (NOB) perform the second step of aerobic nitrification (converting nitrite to nitrate), which is critical for transferring nitrogen to other organisms for assimilation or energy. Despite their ecological importance, there are few cultured or genomic representatives from marine systems. Here, we obtained two NOB (designated as MSP and DJ) enriched from marine sediments and estimated the physiological and genomic traits of these marine microbes. Both NOB enrichment cultures exhibit distinct responses to varying nitrite and salt concentrations. Genomic analyses suggest that these NOB are metabolically flexible (similar to other previously described NOB), and yet also have individual genomic differences that likely support distinct niche distribution. In conclusion, this study provides more insights into the ecological roles of NOB in marine environments.

Giant sulfur bacteria (Beggiatoaceae) from sediments underlying the Benguela upwelling system host diverse microbiomes

“…Neither were members of the Nitrosococcales that were in low abundances in these sediments. DESeq2 found only one statistically significant association between a potential microoxic nitrifier of nitrite to nitrate within an unclassified clade distal to known nitrite nitrifiers within the Nitrospinota [ 164 , 165 ]. This ASV was of low abundance but was clearly enriched in samples from Station 23020, and to a lesser extent, samples from Station GeoChem2_1.…”

Reshaping of bacterial molecular hydrogen metabolism contributes to the outgrowth of commensal E. coli during gut inflammation

“…Hydrogenase activity can be predicted based on primary sequence ( Søndergaard et al, 2016 ). The HydDB database has been widely utilized to classify hydrogenases ( Dong, 2020 ; Mei, 2020 ; Panwar, 2020 ; Park et al, 2020 ; Picone et al, 2020 ; Stairs et al, 2020 ; Wong, 2020 ; Yu et al, 2020 ). We confirmed the reliability of gene annotations in the HydDB database using a simulated metagenomic dataset of hydrogenase-containing and hydrogenase-free genomes (see Materials and methods for details).…”

Metagenomic Views of Microbial Communities in Sand Sediments Associated with Coral Reefs

“…4b). The genes encoding nitrate reductase/nitrite oxidoreductase related to nitrite oxidation were not found in the genome of typical nitrite oxidizing bacteria Nitrospirota (Park, et al 2020) possibly due to genome incompleteness, but in Planctomycetes, Actinobacteriota, Verrucomicrobiota, Methylomirabilota and Gammaproteobacteria. The functional annotations of MAGs also highlighted that members from Proteobacteria (mostly orders of Rhizobiales and Woeseiales) tended to be the most highly metabolically exible (Fig.…”