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Metabolic versatility of aerobic methane-oxidizing bacteria under anoxia in aquatic ecosystems.

ABSTRACT: The potential positive feedback between global aquatic deoxygenation and methane (CH₄) emission emphasizes the importance of understanding CH₄ cycling under O₂-limited conditions. Increasing observations for aerobic CH₄-oxidizing bacteria (MOB) under anoxia have updated the prevailing paradigm that MOB are O₂-dependent; thus, clarification on the metabolic mechanisms of MOB under anoxia is critical and timely. Here, we mapped the global distribution of MOB under anoxic aquatic zones and summarized four underlying metabolic strategies for MOB under anoxia: (a) forming a consortium with oxygenic microorganisms; (b) self-generation/storage of O₂ by MOB; (c) forming a consortium with non-oxygenic heterotrophic bacteria that use other electron acceptors; and (d) utilizing alternative electron acceptors other than O₂. Finally, we proposed directions for future research. This study calls for improved understanding of MOB under anoxia, and underscores the importance of this overlooked CH₄ sink amidst global aquatic deoxygenation.

SUBMITTER: Li B

PROVIDER: S-EPMC11374530 | biostudies-literature | 2024 Oct

REPOSITORIES: biostudies-literature

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Metabolic versatility of aerobic methane-oxidizing bacteria under anoxia in aquatic ecosystems.

Li Biao B Mao Zhendu Z Xue Jingya J Xing Peng P Wu Qinglong L QL

Environmental microbiology reports 20241001 5

The potential positive feedback between global aquatic deoxygenation and methane (CH4) emission emphasizes the importance of understanding CH4 cycling under O2-limited conditions. Increasing observations for aerobic CH4-oxidizing bacteria (MOB) under anoxia have updated the prevailing paradigm that MOB are O2-dependent; thus, clarification on the metabolic mechanisms of MOB under anoxia is critical and timely. Here, we mapped the global dist ...[more]

PMID: 39232853

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Project description: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, currently very few cultured NOB or representative NOB genome sequences from marine environments exist. In this study, we employed enrichment culturing and genomic approaches 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 and 30.0 μM nitrite per day, respectively, with these optimum rates occurring at 0.1 mM and 0.3 mM nitrite, respectively. Each enrichment culture exhibited a different tolerance to various 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 conserved 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 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 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 various nitrite and salt concentrations. Genomic analyses suggest that these NOB are metabolically flexible (similar to other previously described NOB) 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.

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Dataset Information

Metabolic versatility of aerobic methane-oxidizing bacteria under anoxia in aquatic ecosystems.

Publications

Metabolic versatility of aerobic methane-oxidizing bacteria under anoxia in aquatic ecosystems.

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