Wang Shasha, Zhao Zhuoming, Cheng Ruolin, Cui Liang, Wang Jun, Rubin-Blum Maxim, Zhang Yao, Liu Bolin, Chen Xing, Baltar Federico, Cao Xiaxing, Wen Xuezhe, Alain Karine, Chen Zhen, Liao Jing, Jiang Lijing, Shao Zongze
Key Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources of People's Republic of China, Xiamen, 361005, China.
Biology Department, National Institute of Oceanography, Israel Oceanographic and Limnological Research (IOLR), 3108000, Haifa, Israel.
Microbiome. 2025 Sep 1;13(1):194. doi: 10.1186/s40168-025-02177-9.
Mangroves are hotspots of carbon sequestration in transitional zones between marine and terrestrial ecosystems. Microbially driven dark carbon fixation (DCF) is prominent in sediments, yet our understanding of the DCF process across this continuum remains limited. In this study, we explored DCF activities and associated chemoautotrophs along the sediment depth of different mangrove sites in Fujian Province, China, using radiocarbon labeling and molecular techniques.
Our results showed that the DCF rates ranged from 0.02 to 3.27 mmol C m day in all samples, showing a depth-dependent spatial variation. These rates of DCF were closely related to the environmental factors such as DIC, TS, AVS, NH, NO, and NO. Metagenomic analysis revealed six carbon-fixing pathways, with the Calvin-Benson-Bassham (CBB) cycle and Wood-Ljungdahl (WL) pathway being predominant. Further analysis of MAGs revealed that Gammaproteobacteria, Desulfobacteria, and Campylobacteria were the most abundant carbon-fixing groups. Intriguingly, some new lineages were found to have carbon-fixing potential, including two candidatus taxa JAJVIF01 and BMS3Abin14. Metatranscriptomic analyses confirmed that these carbon-fixing microbes were active in situ and occupied different niches. In the surface layers, Gammaproteobacteria with the CBB cycle played an important role in DCF, mainly driven by sulfur and hydrogen oxidation with oxygen reduction; in the deeper layers, Campylobacteria with the reductive tricarboxylic acid (rTCA) cycle and Desulfobacteria with the WL pathway were active members for DCF, mainly through sulfur, hydrogen, and CO oxidation. While in the deepest layers of 18-20 cm, methane-producing archaea Methanosarcinia was the essential member driving DCF. In addition, most taxa containing the WL pathway displayed a mixotrophic lifestyle corresponding to flexible carbon acquisition strategies.
Overall, this study provides new insights into the understanding of biological carbon fixation and its ecological functions in mangrove sediments. Video Abstract.
红树林是海洋和陆地生态系统过渡带中碳固存的热点区域。微生物驱动的暗碳固定（DCF）在沉积物中十分显著，但我们对这一连续体中DCF过程的理解仍然有限。在本研究中，我们利用放射性碳标记和分子技术，探索了中国福建省不同红树林地点沉积物深度上的DCF活动及相关化学自养菌。
我们的结果表明，所有样本中的DCF速率在0.02至3.27 mmol C m² 天之间，呈现出深度依赖性的空间变化。这些DCF速率与溶解无机碳（DIC）、总硫（TS）、酸挥发性硫化物（AVS）、铵（NH₄⁺）、亚硝酸盐（NO₂⁻）和硝酸盐（NO₃⁻）等环境因素密切相关。宏基因组分析揭示了六种碳固定途径，其中卡尔文-本森-巴斯姆（CBB）循环和伍德-Ljungdahl（WL）途径占主导地位。对宏基因组组装基因组（MAGs）的进一步分析表明，γ-变形菌纲、脱硫杆菌纲和弯曲杆菌纲是最丰富的碳固定类群。有趣的是，发现了一些具有碳固定潜力的新谱系，包括两个候选分类单元JAJVIF01和BMS3Abin14。宏转录组分析证实这些碳固定微生物在原位具有活性，并占据不同的生态位。在表层，具有CBB循环的γ-变形菌纲在DCF中起重要作用，主要由硫和氢的氧化以及氧的还原驱动；在较深层，具有还原性三羧酸（rTCA）循环的弯曲杆菌纲和具有WL途径的脱硫杆菌纲是DCF的活跃成员，主要通过硫、氢和CO的氧化。而在18 - 20厘米的最深层，产甲烷古菌甲烷八叠球菌是驱动DCF的关键成员。此外，大多数含有WL途径的分类单元表现出混合营养型生活方式，对应着灵活的碳获取策略。
总体而言，本研究为理解红树林沉积物中的生物碳固定及其生态功能提供了新的见解。视频摘要。
