太湖微生物群落演替对沉水植物残体降解的响应
作者:
作者单位:

1.南京工业大学 生物与制药工程学院,江苏 南京;2.南京师范大学 海洋科学与工程学院,江苏 南京

作者简介:

姚伟:实验操作,数据收集,数据分析,撰写文章,修改文章;宋天顺:提供技术支持,参与论文讨论,审阅文章;宋娜:提出概念,研究设计,获取基金,监督管理,审阅文章。

基金项目:

国家自然科学基金(42377258)


Response of microbial community succession to degradation of submerged plant residues in Taihu Lake
Author:
Affiliation:

1.College of Biotechnology and Pharmaceutical Engineering, Nanjing Tech University, Nanjing, Jiangsu, China;2.College of Marine Science and Engineering, Nanjing Normal University, Nanjing, Jiangsu, China

Fund Project:

This work was supported by the National Natural Science Foundation of China (42377258).

  • 摘要
  • | |
  • 访问统计
  • |
  • 参考文献 [44]
  • |
  • 相似文献 [20]
  • | | |
  • 文章评论
    摘要:

    浅水湖泊沉积物中的有机质降解是调控碳循环与温室气体排放的关键过程,但沉水植物残体降解过程对微生物群落长期演替的调控机制尚未明晰。目的 探究在长时间尺度下沉水植物残体降解对微生物群落的驱动机制。方法 通过4年的微宇宙模拟实验,研究太湖沉积物中竹叶眼子菜(Potamogeton wrightii)残体降解的动态过程,详细解析了有机质组分演变、胞外酶活性对微生物群落演替的动态影响。结果 易降解有机质组分(labile organic matter pool, LP)的快速消耗伴随β-葡萄糖苷酶活性激增,而难降解有机质组分(recalcitrant organic matter pool, RP)累积与酚氧化酶活性滞后响应耦合。微生物群落呈现显著功能分异,芽孢杆菌门(Bacillota)和担子菌门(Basidiomycota)分别主导细菌与真菌群落难降解有机质的降解,揭示了木质素类聚合物降解的代谢分工。方差分解表明易降解有机质与难降解有机质都能独立解释微生物群落差异性,凸显有机质的化学复杂度对功能类群的筛选作用。结论 沉水植物残体降解显著驱动了微宇宙培养体系的微生物群落结构演替,微生物群落组成与有机质组分呈现出协同变化的趋势,并促进了具有不同生长策略的微生物生长。本研究阐明了沉水植物残体降解过程中微生物功能差异与有机质组分复杂度的动态互作规律,为浅水湖泊碳稳定性评估及生态修复提供了理论依据。

    Abstract:

    Organic matter degradation in shallow lake sediments is a key process in regulating the carbon cycle and greenhouse gas emissions, while the mechanism by which submerged plant residue degradation regulates the long-term succession of microbial communities has not yet been clarified.Objective To investigate the mechanisms of microbial community succession driven by submerged plant residue degradation on long time scales.Methods We investigated the degradation dynamics of Potamogeton wrightii residues in Taihu Lake sediments through a 4-year microcosmic simulation experiment and analyzed in detail the dynamic impacts of organic matter fraction evolution and extracellular enzyme activities on microbial community succession.Results The rapid consumption of labile organic matter pool was accompanied by a surge in β- glucosidase activity, while the accumulation of recalcitrant organic matter pool was coupled with a lagged response of phenol oxidase activity. Microbial communities showed significant functional differentiation, with Bacillota and Basidiomycota dominating the degradation of recalcitrant organic matter pool in bacterial and fungal communities, respectively, revealing the metabolic division of labor in the degradation of lignin-like polymers. Variance decomposition showed that both labile and recalcitrant organic matter pools independently explained microbial community variations, highlighting the role of chemical complexity of organic matter in screening functional taxa.Conclusion Degradation of submerged plant residues significantly drove microbial community structure succession in the microcosmic culture system, and microbial community composition and organic matter fractions showed synergistic changes. In addition, the degradation promoted the growth of microorganisms with different growth strategies. This study elucidates the dynamic interactions between microbial functional differences and organic matter pool complexity in the degradation of submerged plant residues, providing a theoretical basis for carbon stability assessment and ecological restoration of shallow lakes.

    参考文献
    [1] GUDASZ C, BASTVIKEN D, STEGER K, PREMKE K, SOBEK S, TRANVIK LJ. Temperature-controlled organic carbon mineralization in lake sediments[J]. Nature, 2010, 466(7305): 478-481.
    [2] 刘新, 黄庆慧, 江和龙, 宋娜. 浅水湖泊沉积物中水生植物残体降解过程及微生物群落变化[J]. 生态环境学报, 2016, 25(3): 489-495.LIU X, HUANG QH, JIANG HL, SONG N. The decomposition processes of aquatic plant residue and the change of microbial community structure in a Shallow Lake sediment[J]. Ecology and Environmental Sciences, 2016, 25(3): 489-495 (in Chinese).
    [3] 徐思南, 吴自军, 张喜林, 孙伟香, 耿威, 曹红, 翟滨, 孙治雷. 海洋沉积物碳循环过程数值模型的研究进展[J]. 地球科学, 2024, 49(4): 1431-1447.XU SN, WU ZJ, ZHANG XL, SUN WX, GENG W, CAO H, ZHAI B, SUN ZL. Advances in Numerical Modelling of Carbon Cycling Processes in Marine Sediments[J]. Earth Science, 2024, 49(4): 1431-1447 (in Chinese).
    [4] SONG N, YAN ZS, CAI HY, JIANG HL. Effect of temperature on submerged macrophyte litter decomposition within sediments from a large shallow and subtropical freshwater lake[J]. Hydrobiologia, 2013, 714(1): 131-144.
    [5] 秦伯强. 浅水湖泊湖沼学与太湖富营养化控制研究[J]. 湖泊科学, 2020, 32(5): 1229-1243.QIN BQ. Shallow lake limnology and control of eutrophication in Lake Taihu[J]. Journal of Lake Sciences, 2020, 32(5): 1229-1243 (in Chinese).
    [6] HU WP, J?RGENSEN SE, ZHANG FB. A vertical-compressed three-dimensional ecological model in Lake Taihu, China[J]. Ecological Modelling, 2006, 190(3-4): 367-398.
    [7] CHENG LJ, XUE B, ZAWISZA E, YAO SC, LIU JL, LI LL. Effects of environmental change on subfossil Cladocera in the subtropical shallow freshwater East Taihu Lake, China[J]. Catena, 2020, 188: 104446.
    [8] 耿荣妹, 胡小贞, 许秋瑾, 冯胜, 薛彦君. 太湖东岸湖滨带水生植物特征及影响因素分析[J]. 环境科学与技术, 2016, 39(12): 17-23.GENG RM, HU XZ, XU QJ, FENG S, XUE YJ. The features of aquatic macrophytes and its influent factors of lakeside zone in the east of Lake Taihu[J]. Environmental Science & Technology, 2016, 39(12): 17-23 (in Chinese).
    [9] LIANG C, SCHIMEL JP, JASTROW JD. The importance of anabolism in microbial control over soil carbon storage[J]. Nature Microbiology, 2017, 2: 17105.
    [10] KOYAMA M, YAMAMOTO S, ISHIKAWA K, BAN S, TODA T. Anaerobic digestion of submerged macrophytes: chemical composition and anaerobic digestibility[J]. Ecological Engineering, 2014, 69: 304-309.
    [11] 徐达, 金伟, 尉艺, 王春柳, 朱伯淞, 化柯, 周攀, 刘新. 沉水植物残体堆积量对沉积物理化性质的影响: 以马来眼子菜为例[J]. 中国环境科学, 2023, 43(3): 1360-1367.XU D, JIN W, WEI Y, WANG CL, ZHU BS, HUA K, ZHOU P, LIU X. The influence of the accumulation of submerged plant residues on the physicochemical properties of sediments: a case study of Malayan cabbage[J]. China Environmental Science, 2023, 43(3): 1360-1367 (in Chinese).
    [12] BANERJEE S, KIRKBY CA, SCHMUTTER D, BISSETT A, KIRKEGAARD JA, RICHARDSON AE. Network analysis reveals functional redundancy and keystone taxa amongst bacterial and fungal communities during organic matter decomposition in an arable soil[J]. Soil Biology and Biochemistry, 2016, 97: 188-198.
    [13] SINSABAUGH RL, HILL BH, FOLLSTAD SHAH JJ. Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment[J]. Nature, 2009, 462(7274): 795-798.
    [14] LI XD, SU LB, JING M, WANG KQ, SONG CG, SONG YL. Nitrogen addition restricts key soil ecological enzymes and nutrients by reducing microbial abundance and diversity[J]. Scientific Reports, 2025, 15: 5560.
    [15] WANG XY, LIANG C, MAO JD, JIANG YJ, BIAN Q, LIANG YT, CHEN Y, SUN B. Microbial keystone taxa drive succession of plant residue chemistry[J]. The ISME Journal, 2023, 17(5): 748-757.
    [16] SHI JW, YANG L, LIAO Y, LI JW, JIAO S, SHANGGUAN ZP, DENG L. Soil labile organic carbon fractions mediate microbial community assembly processes during long-term vegetation succession in a semiarid region[J]. iMeta, 2023, 2(4): e142.
    [17] LEHMANN J, KLEBER M. The contentious nature of soil organic matter[J]. Nature, 2015, 528(7580): 60-68.
    [18] WANG CQ, KUZYAKOV Y. Mechanisms and implications of bacterial-fungal competition for soil resources[J]. The ISME Journal, 2024, 18(1): wrae073.
    [19] LI ZC, LI X, WANG X, MA J, XU J, XU XG, HAN RM, ZHOU YW, YAN XC, WANG GX. Isotopic evidence revealing spatial heterogeneity for source and composition of sedimentary organic matters in Taihu Lake, China[J]. Ecological Indicators, 2020, 109: 105854.
    [20] ROVIRA P, VALLEJO VR. Labile and recalcitrant pools of carbon and nitrogen in organic matter decomposing at different depths in soil: an acid hydrolysis approach[J]. Geoderma, 2002, 107(1-2): 109-141.
    [21] KOURTEV PS, EHRENFELD JG, HUANG WZ. Enzyme activities during litter decomposition of two exotic and two native plant species in hardwood forests of New Jersey[J]. Soil Biology and Biochemistry, 2002, 34(9): 1207-1218.
    [22] CAPORASO JG, LAUBER CL, WALTERS WA, BERG-LYONS D, LOZUPONE CA, TURNBAUGH PJ, FIERER N, KNIGHT R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample[J]. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(supplement_1): 4516-4522.
    [23] GARDES M, BRUNS TD. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts[J]. Molecular Ecology, 1993, 2(2): 113-118.
    [24] REN Y, YU G, SHI CP, LIU LM, GUO Q, HAN C, ZHANG D, ZHANG L, LIU BX, GAO H, ZENG J, ZHOU Y, QIU YH, WEI J, LUO YC, ZHU FJ, LI XJ, WU Q, LI B, FU WY, et al. Majorbio cloud: a one-stop, comprehensive bioinformatic platform for multiomics analyses[J]. iMeta, 2022, 1(2): e12.
    [25] HAN C, SHI CP, LIU LM, HAN JC, YANG QQ, WANG Y, LI XD, FU WY, GAO H, HUANG HS, ZHANG XL, YU KG. Majorbio Cloud 2024: update single-cell and multiomics workflows[J]. iMeta, 2024, 3(4): e217.
    [26] CHEN SF, ZHOU YQ, CHEN YR, GU J. Fastp: an ultra-fast all-in-one FASTQ preprocessor[J]. Bioinformatics, 2018, 34(17): i884-i890.
    [27] MAGO? T, SALZBERG SL. FLASH: fast length adjustment of short reads to improve genome assemblies[J]. Bioinformatics, 2011, 27(21): 2957-2963.
    [28] EDGAR RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads[J]. Nature Methods, 2013, 10(10): 996-998.
    [29] WANG Q, GARRITY GM, TIEDJE JM, COLE JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy[J]. Applied and Environmental Microbiology, 2007, 73(16): 5261-5267.
    [30] SCHLOSS PD, WESTCOTT SL, RYABIN T, HALL JR, HARTMANN M, HOLLISTER EB, LESNIEWSKI RA, OAKLEY BB, PARKS DH, ROBINSON CJ, SAHL JW, STRES B, THALLINGER GG, VAN HORN DJ, WEBER CF. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities[J]. Applied and Environmental Microbiology, 2009, 75(23): 7537-7541.
    [31] SEGATA N, IZARD J, WALDRON L, GEVERS D, MIROPOLSKY L, GARRETT WS, HUTTENHOWER C. Metagenomic biomarker discovery and explanation[J]. Genome Biology, 2011, 12(6): R60.
    [32] 章磊, 徐祎萌, 白美霞, 周燕, 秦华, 徐秋芳, 陈俊辉. 生物质炭配施有机物料对红壤碳组分及酶生态化学计量特征的影响[J]. 浙江农林大学学报, 2024, 41(3): 506-516.ZHANG L, XU YM, BAI MX, ZHOU Y, QIN H, XU QF, CHEN JH. Effects of biochar combined with organic amendments on carbon composition and eco-enzymatic stoichiometry of red soil[J]. Journal of Zhejiang A&F University, 2024, 41(3): 506-516 (in Chinese).
    [33] KIM JI, YANG YR, KANG H. Fluorometric assay for phenol oxidase activity in soils and its controlling variables[J]. Applied Soil Ecology, 2024, 195: 105240.
    [34] YANG ZC, ZHOU Q, SUN HM, JIA LX, ZHAO L, WU WZ. Metagenomic analyses of microbial structure and metabolic pathway in solid-phase denitrification systems for advanced nitrogen removal of wastewater treatment plant effluent: a pilot-scale study[J]. Water Research, 2021, 196: 117067.
    [35] MANICI LM, CAPUTO F, de SABATA D, FORNASIER F. The enzyme patterns of Ascomycota and Basidiomycota fungi reveal their different functions in soil[J]. Applied Soil Ecology, 2024, 196: 105323.
    [36] ZHALNINA K, LOUIE KB, HAO Z, MANSOORI N, ROCHA UN DA, SHI SJ, CHO H, KARAOZ U, LOQUé D, BOWEN BP, FIRESTONE MK, NORTHEN TR, BRODIE EL. Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly[J]. Nature Microbiology, 2018, 3(4): 470-480.
    [37] FERNANDES CG, SAWANT SC, MULE TA, KHADYE VS, LALI AM, ODANETH AA. Enhancing cellulases through synergistic β-glucosidases for intensifying cellulose hydrolysis[J]. Process Biochemistry, 2022, 120: 202-212.
    [38] ZHANG ZX, HAO M, YU QH, DUN XJ, XU JW, GAO P. The effect of thinning intensity on the soil carbon pool mediated by soil microbial communities and necromass carbon in coastal zone protected forests[J]. Science of the Total Environment, 2023, 881: 163492.
    [39] CHEN RR, SENBAYRAM M, BLAGODATSKY S, MYACHINA O, DITTERT K, LIN XG, BLAGODATSKAYA E, KUZYAKOV Y. Soil C and N availability determine the priming effect: microbial N mining and stoichiometric decomposition theories[J]. Global Change Biology, 2014, 20(7): 2356-2367.
    [40] SONG N, JIANG HL. Coordinated photodegradation and biodegradation of organic matter from macrophyte litter in shallow lake water: dual role of solar irradiation[J]. Water Research, 2020, 172: 115516.
    [41] DE BOER W, FOLMAN LB, SUMMERBELL RC, BODDY L. Living in a fungal world: impact of fungi on soil bacterial niche development[J]. FEMS Microbiology Reviews, 2005, 29(4): 795-811.
    [42] SUBIRATS J, SHARPE H, TOPP E. Fate of Clostridia and other spore-forming Firmicute bacteria during feedstock anaerobic digestion and aerobic composting[J]. Journal of Environmental Management, 2022, 309: 114643.
    [43] HE MQ, CAO B, LIU F, BOEKHOUT T, DENCHEV TT, SCHOUTTETEN N, DENCHEV CM, KEMLER M, GORJóN SP, BEGEROW D, VALENZUELA R, DAVOODIAN N, NISKANEN T, VIZZINI A, REDHEAD SA, RAMíREZ-CRUZ V, PAPP V, DUDKA VA, DUTTA AK, GARCíA-SANDOVAL R, et al. Phylogenomics, divergence times and notes of orders in Basidiomycota[J]. Fungal Diversity, 2024, 126(1): 127-406.
    [44] MATANGE K, RAJAEI V, CAPERA-ARAGONES P, COSTNER JT, ROBERTSON A, KIM JS, PETROV AS, BOWMAN JC, WILLIAMS LD, FRENKEL-PINTER M. Evolution of complex chemical mixtures reveals combinatorial compression and population synchronicity[J]. Nature Chemistry, 2025, 17(4): 590-597.
    引证文献
    网友评论
    网友评论
    分享到微博
    发 布
引用本文

姚伟,宋天顺,宋娜. 太湖微生物群落演替对沉水植物残体降解的响应[J]. 微生物学报, 2025, 65(6): 2688-2704

复制
分享
文章指标
  • 点击次数:28
  • 下载次数: 161
  • HTML阅读次数: 32
  • 引用次数: 0
历史
  • 收稿日期:2025-03-23
  • 在线发布日期: 2025-06-05
文章二维码