Molecular and stable isotopic evidence for the occurrence of nitrite-dependent anaerobic methane-oxidizing bacteria in the mangrove sediment of Zhangjiang Estuary, China

Abstract

Nitrite-dependent anaerobic methane oxidation (n-damo), which is mediated by "Candidatus Methylomirabilis oxyfera-like" bacteria, is unique in linking the carbon and nitrogen cycles. However, the niche and activity of n-damo bacteria in the mangrove ecosystem have not been confirmed. Here, we report the occurrence of the n-damo process in the mangrove wetland of the Zhangjiang Estuary, China. The widespread occurrence of n-damo bacteria in mangrove wetland was confirmed using real-time quantitative polymerase chain reaction (qPCR) assay, which showed that the abundance of Methylomirabilis oxyfera-like bacterial 16S rRNA and pmoA genes ranged from 2.43 × 10 to 2.09 × 10 and 2.07 × 10 to 3.38 × 10copies per gram of dry soil in the examined sediment cores. The highest amount of targeting genes was all detected in the upper layer (0-20 cm). Phylogenetic analyses of n-damo bacterial 16S rRNA and pmoA genes illustrated the depth-specific distribution and high diversity of n-damo bacteria in the mangrove wetland. Stable isotope experiments further confirmed the occurrence of n-damo in the examined mangrove sediments, and the potential n-damo rates ranged from 25.93 to 704.08 nmol CO per gram of dry soil per day at different depths of the sediment cores, with the n-damo being more active in the upper layer of the mangrove sediments. These results illustrate the existence of active M. oxyfera-like bacteria and indicate that the n-damo process is a previously overlooked microbial methane sink in the mangrove wetlands.

Processes and Microorganisms Involved in the Marine Nitrogen Cycle: Knowledge and Gaps

“…− and CH 4 concentrations, suggesting that anaerobic NH 4 + oxidation is coupled to NO 3 − reduction and denitrification (Padilla et al, 2016;Thamdrup et al, 2019). M. oxyfera-like bacteria have also been detected in estuarine and coastal sediments, where they show great diversity and a depth-specific distribution influenced by redox potential, water content and total organic C (Lidong et al, 2014;Zhang et al, 2018). Moreover, the activity of this community in coastal sediments vary seasonally and spatially and seem to be highly influenced by NO 3 − (Shen et al, 2016;Wang et al, 2017), NH 4 + , NO 2 − (Chen et al, 2014(Chen et al, , 2015b and salinity (Chen et al, 2015a;Shen et al, 2016).…”

Nitrogen Cycling and Mass Balance in the World’s Mangrove Forests

“…Several microbial groups and transformation processes have only recently been discovered (DNRA, anammox, methane denitrification), but are often quantitatively important in N cycling. For example, a nitrite-dependent anaerobic methane-oxidizing bacterium was recently discovered in mangrove soils of the Zhangjiang estuary in China [128]. This "Candidatus Methylomirabilis oxyfera-like" bacterium is unique in linking the carbon and nitrogen cycles.…”

Depth-related Variability of Biological Nitrogen Fixation and Diazotrophic Communities in Mangrove Sediments

“…However, the uptake of ammonium and nitrate by plants was down regulated under carbon limiting conditions [77]. Therefore, in deep mangrove sediments with low organic carbon content [78], the main form of nitrogen uptaken by mangrove species was assumed to be amino acids. In support of this assumption, our metagenomic sequencing analysis showed that with the increasing depth of mangrove sediments, both biological nitrogen xation and ammonia assimilation pathways were enhanced, whereas ammonia and organic nitrogen loss by denitri cation and organic nitrogen decomposition pathways was weakened.…”