Microbial carbon use efficiency governs the accumulation of microbial-derived carbon in restored mangroves

doi:10.1093/jpe/rtaf230

J Plant Ecol ›› 2026, Vol. 19 ›› Issue (4): rtaf230.DOI: 10.1093/jpe/rtaf230

• Research Articles • Previous Articles

Microbial carbon use efficiency governs the accumulation of microbial-derived carbon in restored mangroves

Xingyun Huang^1,2, Fangyuan Guan¹, Zhe Lu¹, Guoming Qin¹, Yongxing Cui³, Tao Li⁴, Evans Asenso⁵, Ruichang Shen⁶, Benjamin J. Wainwright⁷, Jingwei Shi¹, Lulu Zhang¹, Hui Li⁸, Jingfan Zhang^1,2, Jinge Zhou^1,2, Ruyi Ding^1,2, Hua He^1,2 and Faming Wang^1,*

¹Guangdong Provincial Key Laboratory of Applied Botany, Xiaoliang Research Station for Tropical Coastal Ecosystems, and Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China
²University of Chinese Academy of Sciences, Beijing 100049, China
³Institute of Biology, Freie Universität Berlin, Berlin 14195, Germany
⁴Department of Microbiology and Ecosystem Science, Division of Terrestrial Ecosystem Research, Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna A-1030, Austria
⁵Department of Agricultural Engineering, School of Engineering Sciences, University of Ghana, Accra 00202, Ghana
⁶Key Laboratory of Poyang Lake Environment and Resource Utilization, Ministry of Education, Center for Watershed Ecology, School of Life Science, Nanchang University, Nanchang 330031, China
⁷Yale-NUS College, National University of Singapore, Kent Ridge 119077, Singapore
⁸Guangdong Eco-engineering Polytechnic, Guangzhou 510520, China
^*Corresponding author. E-mail: wangfm@scbg.ac.cn

Received:2025-05-27 Accepted:2025-12-20 Published:2026-08-01
Supported by:
This study was funded by the Alliance of National and International Science Organizations for the Belt and Road Regions (ANSO-CR-KP-2022-11), the CAS Project for Young Scientists in Basic Research (YSBR-037), the MOST Ocean Negative Carbon Emissions Project, National Key R&D Program of China (2023YFE0113100 and 2023YFF1304500), Key Special Project for Marine Environmental Security and Sustainable Development of Coral Reefs (2021-400), the National Natural Science Foundation of China (42471067 and U2106209), Guangdong Basic and Applied Basic Research Foundation (2023A1515010946), the CAS Youth Innovation Promotion Association (2021347), the National Forestry and Grassland Administration Youth Talent Support Program (2020BJ003), Key-Area Research and Development Program of Guangdong Province (2022B1111230001), Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai) (SML2023SP218) and Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden (2023B1212060046).

微生物碳利用效率驱动红树林恢复过程中微生物源碳的积累

Abstract

Abstract: While mangrove restoration has a great potential for enhancing soil organic carbon (SOC) sequestration in coastal wetlands, microbial-mediated SOC decomposition introduces huge uncertainty to this process. Microbial carbon use efficiency (CUE) is a crucial trait for microorganisms controlling SOC turnover, but how mangrove restoration could affect microbial CUE remains unclear. Here, we investigated the effects of mangrove restoration on microbial CUE in a typical restored mangrove wetland and further explored its connection to microbial necromass carbon (MNC) content. Our results revealed mangrove restoration increased microbial CUE by 37.84%–56.76% due to an increase in organic carbon quality and a shift in microbial community structure from fast-growing r-strategist (bacteria-dominated including Proteobacteria and Bacteroidota) to slow-growing K-strategist (fungal taxa and bacterial phyla such as Actinobacteriota, Acidobacteriota, and Chloroflexi). Microbial CUE was also positively correlated with MNC, explaining 73% and 69% variations in fungal and bacterial necromass C, respectively. These findings indicate that mangrove restoration enhances SOC sequestration not only through increased plant-derived carbon input but also by elevating microbial CUE and promoting MNC accumulation. Although bacterial necromass carbon showed a higher percentage increase, fungal necromass constituted the dominant portion of the accrued microbial-derived carbon pool, underscoring the critical role of fungal communities in the formation of stable SOC. Our study highlights the significant role of microbial processes in promoting SOC accumulation during mangrove restoration. These results emphasize the importance of incorporating microbial processes into coastal wetland restoration strategies to maximize C sequestration.

Mangrove restoration significantly enhances microbial carbon use efficiency and promotes microbial necromass carbon accumulation by improving organic carbon quality and driving a shift in microbial community from r-strategists to K-strategists. These findings highlight the importance of incorporating microbial processes into restoration strategies to maximize soil organic carbon sequestration in coastal wetlands.

Key words: mangroves, carbon use efficiency, carbon sequestration, microbial life strategist, microbial necromass

摘要：
红树林恢复在提升滨海湿地土壤有机碳固存能力方面具有巨大潜力。微生物碳利用效率(CUE)是调控土壤有机碳周转的关键微生物性状，但红树林恢复如何影响微生物CUE及其碳固存效应仍不清楚。本研究以典型红树林恢复湿地为对象，探究红树林恢复对CUE的影响，并揭示其与微生物残体碳积累之间的关联。结果表明，红树林恢复使CUE提升了37.84%–56.76%，这主要归因于有机碳质量的提高以及微生物群落从r-策略(细菌主导，包括变形菌门和拟杆菌门)向K-策略类群(真菌类群及放线菌门、酸杆菌门、绿弯菌门等细菌门类)的转变。微生物CUE与残体碳含量呈正相关，分别解释了真菌和细菌残体碳73%和69%的变异。上述结果表明，红树林恢复不仅增加植物来源的碳输入，还通过提高微生物CUE和促进残体碳积累来增强土壤有机碳固存。在本研究中，尽管细菌残体碳的增幅更高，但真菌残体在新积累的微生物源碳库中占主导地位，凸显了真菌群落在土壤有机碳稳定中的关键作用。本研究揭示了红树林恢复过程中，微生物在驱动土壤有机碳累积的重要作用。综上所述，在滨海湿地恢复策略中，纳入微生物调控过程对于最大化碳固存至关重要。

关键词: 红树林, 碳利用效率, 碳固持, 微生物生活史策略, 微生物残体

Xingyun Huang, Fangyuan Guan, Zhe Lu, Guoming Qin, Yongxing Cui, Tao Li, Evans Asenso, Ruichang Shen, Benjamin J. Wainwright, Jingwei Shi, Lulu Zhang, Hui Li, Jingfan Zhang, Jinge Zhou, Ruyi Ding, Hua He, Faming Wang. Microbial carbon use efficiency governs the accumulation of microbial-derived carbon in restored mangroves[J]. J Plant Ecol, 2026, 19(4): 1-.

[1]	Yushu Tian, Pin Li, Chenhan Ma, Yun Li, Qiannan Lin, Xiaofan Hou, Xilin Yuan, Xiaotong Zhu, Congcong Shen. Tree species and urban green space types jointly drive rhizosphere SOC fractionation and stability via microbial-enzymatic pathways [J]. J Plant Ecol, 2026, 19(3): 0-.
[2]	Zixuan Zhou, Jie Li, Xuezheng Han, Weifeng Gao, Nianpeng He. Changes in four-dimensional carbon sinks in forest ecosystems: Evidence from the Heilongjiang Province of China [J]. J Plant Ecol, 2026, 19(3): 1-.
[3]	Yarong Sun, Jian Li, Guowei Liang, Yunming Chen. Planting density modulates soil organic carbon sources by regulating plant lignin and microbial necromass C in temperate forests [J]. J Plant Ecol, 2026, 19(2): 1-.
[4]	Yu-Lin Zhang, Wang Xiang, Xiang-Rong Cheng. Stand density–induced tree species diversity alters microbial carbon fixation/degradation genes and soil organic carbon pool during forest rewilding [J]. J Plant Ecol, 2026, 19(2): 1-.
[5]	Qingquan Xie, Yongxian Liu, Zihong Zhu, Kongcao Xiao, Dejun Li. Depth-dependent mechanisms underpinning soil organic carbon accumulation following afforestation [J]. J Plant Ecol, 2026, 19(2): 1-.
[6]	Qiongwei Lei, Xiaoyan Kang, Mingxu Li, Nianpeng He. Divergent responses of photosynthesis and respiration underlie the nonlinear response of carbon use efficiency to temperature in sub-frigid forest in China [J]. J Plant Ecol, 2026, 19(1): 1-.
[7]	Dandan Zhang, Jinsheng Li, Zhen Zhang, Xiaoli Cheng. Drivers of microbial necromass carbon and its contribution to soil organic carbon along an elevational gradient [J]. J Plant Ecol, 2025, 18(6): 1-37.
[8]	Shiwen Ding, Fons van der Plas, Jie Li, Bai Liu, Man Xu, Tongtong Xu, Xiaobin Pan, Qing Chang, Ying Chen, Yinong Li. Grazing effects on the relationship between plant functional diversity and soil carbon sequestration regulated by livestock species [J]. J Plant Ecol, 2024, 17(5): 1-12.
[9]	Yang Lin, Jiang-Tao Xiao, Yong-Ping Kou, Jia-Xing Zu, Xin-Ran Yu, Yuan-Yuan Li. Aboveground carbon sequestration rate in alpine forests on the eastern Tibetan Plateau: impacts of future forest management options [J]. J Plant Ecol, 2023, 16(3): 0-rtad001.
[10]	Zhiyong Zhou, Ying Shen, Bo Wang and Huan Zhang. Soil calcium content as the driving factor for vegetative structure and soil microbial function diverging across a fire chronosequence of the boreal forests in northeast China [J]. J Plant Ecol, 2022, 15(2): 372-384.
[11]	Sridevi Ravi, Martin K.-F. Bader, Tim Young, Mark Duxbury, Michael Clearwater, Cate Macinnis-Ng and Sebastian Leuzinger. Are the well-fed less thirsty? Effects of drought and salinity on New Zealand mangroves [J]. J Plant Ecol, 2022, 15(1): 85-99.
[12]	Singkone Xayalath, Isao Hirota, Shinsuke Tomita and Michiko Nakagawa. Aboveground biomass and seasonal patterns of aboveground net primary productivity in five bamboo species in northern Laos [J]. J Plant Ecol, 2020, 13(2): 150-156.
[13]	Enzai Du, Zhang Zhou, Peng Li, Xueyang Hu, Yuecun Ma, Wei Wang, Chengyang Zheng, Jianxiao Zhu, Jin-Sheng He, Jingyun Fang. NEECF: a project of nutrient enrichment experiments in China's forests [J]. J Plant Ecol, 2013, 6(5): 428-435.
[14]	Wenhong Li, Pengfei Zhang, Jiansheng Ye, Laifang Li, Paul A. Baker. Impact of two different types of El Niño events on the Amazon climate and ecosystem productivity [J]. J Plant Ecol, 2011, 4(1-2): 91-99.
[15]	Zhongkui Luo, Osbert Jianxin Sun, Hualin Xu. A comparison of species composition and stand structure between planted and natural mangrove forests in Shenzhen Bay, South China [J]. J Plant Ecol, 2010, 3(3): 165-174.

Microbial carbon use efficiency governs the accumulation of microbial-derived carbon in restored mangroves

微生物碳利用效率驱动红树林恢复过程中微生物源碳的积累

HTML

PDF

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 15

Recommended Articles

Metrics

Comments