Environmental Microbiomics Research Center, School of Environmental Science and Engineering, Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), State Key Laboratory of Biocontrol, Sun Yat-Sen University, Guangzhou, 510006, China.
Department of Civil and Environmental Engineering, the University of Tennessee, Knoxville, TN, 37996, USA.
Microbiome. 2023 Apr 5;11(1):71. doi: 10.1186/s40168-023-01501-5.
Mangrove ecosystems are considered as hot spots of biogeochemical cycling, yet the diversity, function and coupling mechanism of microbially driven biogeochemical cycling along the sediment depth of mangrove wetlands remain elusive. Here we investigated the vertical profile of methane (CH), nitrogen (N) and sulphur (S) cycling genes/pathways and their potential coupling mechanisms using metagenome sequencing approaches.
Our results showed that the metabolic pathways involved in CH, N and S cycling were mainly shaped by pH and acid volatile sulphide (AVS) along a sediment depth, and AVS was a critical electron donor impacting mangrove sediment S oxidation and denitrification. Gene families involved in S oxidation and denitrification significantly (P < 0.05) decreased along the sediment depth and could be coupled by S-driven denitrifiers, such as Burkholderiaceae and Sulfurifustis in the surface sediment (0-15 cm). Interestingly, all S-driven denitrifier metagenome-assembled genomes (MAGs) appeared to be incomplete denitrifiers with nitrate/nitrite/nitric oxide reductases (Nar/Nir/Nor) but without nitrous oxide reductase (Nos), suggesting such sulphide-utilizing groups might be an important contributor to NO production in the surface mangrove sediment. Gene families involved in methanogenesis and S reduction significantly (P < 0.05) increased along the sediment depth. Based on both network and MAG analyses, sulphate-reducing bacteria (SRB) might develop syntrophic relationships with anaerobic CH oxidizers (ANMEs) by direct electron transfer or zero-valent sulphur, which would pull forward the co-existence of methanogens and SRB in the middle and deep layer sediments.
In addition to offering a perspective on the vertical distribution of microbially driven CH, N and S cycling genes/pathways, this study emphasizes the important role of S-driven denitrifiers on NO emissions and various possible coupling mechanisms of ANMEs and SRB along the mangrove sediment depth. The exploration of potential coupling mechanisms provides novel insights into future synthetic microbial community construction and analysis. This study also has important implications for predicting ecosystem functions within the context of environmental and global change. Video Abstract.
红树林生态系统被认为是生物地球化学循环的热点，但红树林湿地沉积物深度上微生物驱动的生物地球化学循环的多样性、功能和耦合机制仍不清楚。在这里，我们使用宏基因组测序方法研究了甲烷 (CH)、氮 (N) 和硫 (S) 循环基因/途径的垂直分布及其潜在的耦合机制。
我们的研究结果表明，参与 CH、N 和 S 循环的代谢途径主要受 pH 和酸可挥发性硫 (AVS) 沿沉积物深度的影响，AVS 是影响红树林沉积物 S 氧化和反硝化的关键电子供体。S 氧化和反硝化相关的基因家族沿沉积物深度显著减少（P < 0.05），并且可以通过表面沉积物（0-15 cm）中的硫驱动反硝化菌（如伯克霍尔德氏菌和 Sulfurifustis）耦合。有趣的是，所有硫驱动反硝化菌的宏基因组组装基因组 (MAG) 似乎都是不完全反硝化菌，具有硝酸盐/亚硝酸盐/一氧化氮还原酶（Nar/Nir/Nor）但没有一氧化二氮还原酶（Nos），表明这些利用硫的群体可能是表面红树林沉积物中 NO 产生的重要贡献者。参与甲烷生成和 S 还原的基因家族沿沉积物深度显著增加（P < 0.05）。基于网络和 MAG 分析，硫酸盐还原菌 (SRB) 可能通过直接电子转移或零价硫与厌氧 CH 氧化菌 (ANMEs) 建立共生关系，这将推动产甲烷菌和 SRB 在中深层沉积物中的共存。
本研究除了提供微生物驱动的 CH、N 和 S 循环基因/途径垂直分布的视角外，还强调了硫驱动反硝化菌对 NO 排放的重要作用以及 ANMEs 和 SRB 沿红树林沉积物深度的各种可能耦合机制。对潜在耦合机制的探索为未来合成微生物群落的构建和分析提供了新的思路。本研究对预测环境和全球变化背景下的生态系统功能也具有重要意义。
