Effects of Spartina alterniflora invasion on ammonia-oxidizing microbial communities in marsh soils of the Min River estuary
CHEN Bing-bing1,2, SUN Zhi-gao2,3, WU Hui-hui2,3, WANG Xiao-ying2,3, MAO Li2,3, LI Yan-zhe2,3
1. College of Tourism, Resources and Environment, Zaozhuang University, Zaozhuang 277000, China; 2. Fujian Provincial Key Laboratory for Subtropical Resources and Environment, Fujian Normal University, Fuzhou 350007, China; 3. Key Laboratory of Humid Subtropical Eco-geographical Process (Fujian Normal University), Ministry of Education, Fuzhou 350007, China
Abstract：To explore the differences in community structure and diversity of ammonia-oxidizing archaea (AOA) and ammonia- oxidizing bacteria (AOB) in marsh soils at different invasion stages of Spartina alterniflora, the mudflat (BF, before invasion) and the S. alterniflora marsh after seaward invasion for 1~2 years (SA M) and 6~7 years (SAM) in Shanyutan of the Min River estuary were investigated by the high-throughput sequencing method. Results showed that, as affected by S. alterniflora invasion, the richness and diversity (represented by OTUs, Chao1index and Shannon index) of AOA in marsh soils were significantly higher than those of AOB. The seaward invasion of S. alterniflora reduced the richness of AOA (represented by OTUs and Chao1index) and the diversity of AOB (represented by Shannon index), but increased the diversity of AOA and the richness of AOB in marsh soils. The AOA in soils of different invasion stages was predominated by Thaumarchaeota. Differently, the AOB in soils of BF and SAM were predominated by Crenarchaeota (>90%), while those of SAM was predominated by Pseudomonadota. Nitrosopumilus was the dominant bacterial genus in AOA and its relative abundance in soils of different invasion stages exceeded 98%. By comparison the unclassified bacterial genera were the dominant bacterial genus in AOB and its relative abundance in soils at different invasion stages exceeded 90%. The seaward invasion of S. alterniflora increased the spatial heterogeneity of microbial community composition among samples in marsh soils (especially AOB), which was primarily due to the increased spatial heterogeneity of environmental factors caused by strong siltation of S. alterniflora. This study found that the AOA predominated the process of ammonia oxidation in soils of different seaward invasion stages of S. alterniflora. The seaward invasion of S. alterniflora altered the physio-chemical properties (e.g., pH and EC) and N nutrient conditions in marsh soils, which greatly influenced the structure and diversity of ammonia-oxidizing microbial communities.
陈冰冰, 孙志高, 武慧慧, 王晓颖, 毛立, 厉彦哲. 互花米草入侵对闽江口湿地土壤氨氧化微生物群落的影响[J]. 中国环境科学, 2024, 44(4): 2309-2319.
CHEN Bing-bing, SUN Zhi-gao, WU Hui-hui, WANG Xiao-ying, MAO Li, LI Yan-zhe. Effects of Spartina alterniflora invasion on ammonia-oxidizing microbial communities in marsh soils of the Min River estuary. CHINA ENVIRONMENTAL SCIENCECE, 2024, 44(4): 2309-2319.
[1] Sun Z G, Sun W G, Tong C, et al. China's coastal wetlands:Conservation history, implementation efforts, existing issues and strategies for future improvement[J]. Environment International, 2015, 79:25-41. [2] Galloway J N, Dentener F J, Capone D G, et al. Nitrogen cycles:past, present, and future[J]. Biogeochemistry, 2004,70(2):153-226. [3] Lin X, Zheng P, Zou S, et al. Seagrass (Zostera marina) promotes nitrification potential and selects specific ammonia oxidizers in coastal sediments[J]. Journal of Soils and Sediments, 2021,21(10):3259-3273. [4] Prosser J I, Hink L, Gubry-Rangin C, et al. Nitrous oxide production by ammonia oxidizers:Physiological diversity, niche differentiation and potential mitigation strategies[J]. Global Chang Biology, 2020, 26(1):103-118. [5] Liu H, Hu H, Huang X, et al. Canonical ammonia oxidizers, rather than comammox Nitrospira, dominated autotrophic nitrification during the mineralization of organic substances in two paddy soils[J]. Soil Biology and Biochemistry, 2021,156:108192. [6] Hu L, Dong Z X, Wang Z, et al. The contributions of ammonia oxidizing bacteria and archaea to nitrification‑dependent N2O emission in alkaline and neutral purple soils[J]. Scientific Reports, 2022,12:19928. [7] He C Q, Wang X X, Wang D Y, et al. Impact of Spartina alterniflora invasion on soil bacterial community and associated greenhouse gas emission in the Jiuduansha wetland of China[J]. Applied Soil Ecology, 2021,168:104168. [8] Yang W, An S Q, Zhao H, et al. Impacts of Spartina alterniflora invasion on soil organic carbon and nitrogen pools sizes, stability, and turnover in a coastal salt marsh of eastern China[J]. Ecological Engineering, 2016,86:174-182. [9] Gao D, Li X, Lin X, et al. Soil dissimilatory nitrate reduction processes in the Spartina alterniflora invasion chronosequences of a coastal wetland of southeastern China:dynamics and environmental implications[J]. Plant and Soil, 2017,421(1/2):383-399. [10] Li N I, Li B, Nie M, et al. Effects of exotic Spartina alterniflora on saltmarsh nitrogen removal in the Yangtze River Estuary, China[J]. Journal of Cleaner Production, 2020,271:122557. [11] Bernhard A E, Bollmann A. Estuarine nitrifiers:new players, patterns and processes[J]. Estuarine Coastal and Shelf Science, 2010,88:1-11. [12] Chen S T, Gao D Z, Zhang J B, et al. Invasive Spartina alterniflora accelerates soil gross nitrogen transformations to optimize its nitrogen acquisition in an estuarine and coastal wetland of China[J]. Soil Biology and Biochemistry, 2022,174:108835. [13] Zhang C B, Liu W L, Luo B, et al. Spartina alterniflora invasion impacts denitrifying community diversity and functioning in marsh soils[J]. Geoderma, 2020,375:114456. [14] 刘志君,崔丽娟,李伟,等.互花米草入侵对盐城滨海湿地nirS型反硝化细菌多样性及群落结构的影响[J]. 生态环境学报, 2022,31(4):704-714. Liu Z J, Cui L J, Li W, et al. Effects of Spartina alterniflora invasion on the diversity and community structure of nirS-type denitrifying bacteria in Yancheng coastal wetlands[J]. Ecology and Environmental Sciences, 2022,31(4):704-714. [15] 童晓雨,孙志高,曾阿莹,等.闽江河口互花米草海向入侵对湿地土壤无机硫赋存形态的影响[J]. 应用生态学报, 2019,30(10):3518-3526. Tong X Y, Sun Z G, Zeng A Y, et al. Effects of Spartina alterniflora invasion in a seaward direction on variations of inorganic sulfur forms in marsh soils of the Minjiang River estuary, China[J]. Chinese Journal of Applied Ecology, 2019,30(10):3518-3526. [16] 林少颖,陈桂香,刘旭阳,等.互花米草入侵对河口湿地土壤细菌群落结构及多样性影响[J]. 环境科学学报, 2020,40(8):3001-3012. Lin S Y, Chen G X, Liu X Y, et al. Effects of Spartina alterniflora invasion on soil bacterial community structure and diversity in estuarine wetland[J]. Acta Scientiae Circumstantiae, 2022,40(8):3001-3012. [17] 尹晓雷,陈桂香,王纯,等.互花米草入侵对河口湿地土壤真菌群落结构及多样性影响[J]. 环境科学学报, 2020,40(6):2186-2194. Yin X L, Chen G X, Wang C, et al. Effects of Spartina alterniflora invasion on soil fungi community structure and diversity in estuarine wetland[J]. Acta Scientiae Circumstantiae, 2022,40(6):2186-2194. [18] 陈冰冰,孙志高,胡星云,等.闽江河口互花米草不同入侵阶段湿地土壤nirK型反硝化微生物群落结构及多样性[J]. 应用生态学报, 2022a,33(11):3007-3015. Chen B B, Sun Z G, Hu X Y, et al. Structure and diversity of nirK-type denitrifying microbial community in marsh soils at different invasion stages of Spartina alterniflora in the Minjiang River estuary[J]. Chinese Journal of Applied Ecology, 2022a,33(11):3007-3015. [19] 陈冰冰,孙志高,胡星云,等.闽江河口互花米草海向入侵对湿地土壤nirS型反硝化微生物群落结构及多样性的影响[J]. 环境科学学报, 2022b,42(4):443-453. Chen B B, Sun Z G, Hu X Y, et al. Effects of Spartina alterniflora invasion in a seaward direction on structure and diversity of nirS-type denitrifying microbial community in marsh soils of the Min River estuary[J]. Acta Scientiae Circumstantiae, 2022b,42(4):443-453. [20] 陈钰,郑毅,王晓彤,等.互花米草入侵对河口湿地铁还原菌群落结构及多样性影响[J]. 环境科学学报, 2020,40(12):4570-4580. Chen Y, Zheng Y, Wang X T, et al. Effects of Spartina alterniflora invasion on iron-reducing bacteria community structure and diversity in estuarine wetland[J]. Acta Scientiae Circumstantiae, 2020,40(12):4570-4580. [21] 曾庆淞,陈钰,郑毅,等.互花米草入侵对河口湿地土壤环境中铁氧化菌群落结构及多样性影响[J]. 环境科学学报, 2022,42(5):425-434. Zeng Q S, Chen Y, Zheng Y, et al. Effects of Spartina alterniflora invasion on soil iron-oxidizing bacteria community structure and diversity in estuarine wetland[J]. Acta Scientiae Circumstantiae, 2022, 42(5):425-434. [22] Francis C A, Roberts K J, Beman J M, et al. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean[J]. PNAS, 2005,102:14683-14688. [23] Wang H T, Su J Q, Zheng T L, et al. Insights into the role of plant on ammonia-oxidizing bacteria and archaea in the mangrove ecosystem[J]. Journal of Soils and Sediments, 2015,15(5):1212-1223. [24] 刘文莉,张崇邦,刘亮,等.氨氧化基因丰度和潜在氨氧化速率对加拿大一枝黄花入侵和土壤类型的响应[J]. 植物营养与肥料学报, 2020,26(7):1367-1374. Liu W L, Zhang C B, Liu L, et al. Responses of soil ammonia-oxidizing gene abundances and potential ammonia-oxidizing rate to Solidago canadensis invasion and soil types[J]. Journal of Plant Nutrition and Fertilizers, 2020,26(7):1367-1374. [25] Philippot L, Raaijmakers J M, Lemanceau P, et al. Going back to the roots:The microbial ecology of the rhizosphere[J]. Nature Reviews Microbiology, 2013,11(11):789-799. [26] Qi X E, Wang C, He T J, et al. Changes in alpine grassland type drive niche differentiation of nitrifying communities on the Qinghai-Tibetan Plateau[J]. European Journal of Soil Biology, 2021,104:103316. [27] Cao M M, Cui L N, Sun H M,et al. Effects of Spartina alterniflora invasion on soil microbial community structure and ecological functions[J]. Microorganisms, 2021,9(1):138. [28] 邹温馨,苏卫华,陈远学,等.长期施氮对酸性紫色土氨氧化微生物群落及其硝化作用的影响[J]. 中国农业科学, 2022,55(3):529-542. Zou W X, Su W H, Chen Y X, et al. Effects of Long-term nitrogen application on ammonia oxidizer communities for nitrification in acid purple soil[J]. Scientia Agricultura Sinica, 2022,55(3):529-542. [29] Zhalnina K, de Quadros P D, Camargo F A, et al. Drivers of archaeal ammonia-oxidizing communities in soil[J]. Frontiers in Microbiology, 2012,3:210. [30] Prosser J I, Nicol G W. Archaeal and bacterial ammonia-oxidisers in soil:the quest for niche specialisation and differentiation[J]. Trends in Microbiology, 2012,20:523-531. [31] Uygur A. Specific nutrient removal rates in saline wastewater treatment using sequencing batch reactor[J]. Process Biochemistry, 2006,41:61-66. [32] Bernhard A E, Tucker J, Giblin A E, et al. Functionally distinct communities of ammonia-oxidizing bacteria along an estuarine salinity gradient[J]. Environmental Microbiology, 2007,9(6):1439-1447. [33] Shen J P, Zhang L M, Di H J, et al. A review of ammonia-oxidizing bacteria and archaea in Chinese soils[J]. Frontiers in Microbiology, 2012,3:296. [34] Jin T, Zhang T, Ye L, et al. Diversity and quantity of ammonia-oxidizing archaea and bacteria in sediment of the Pearl River estuary, China[J]. Applied Microbiology and Biotechnology, 2011,90:1137-1145. [35] Hallam S J, Mincer T J, Schleper C, et al. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine crenarchaeota[J]. PLoS Biology, 2006, 4:520-536. [36] Mosier A C, Francis C A. Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary[J]. Environmental Microbiology, 2008,10:3002-3016. [37] Zhang Y, Chen L J, Sun R H, et al. Population and diversity of ammonia-oxidizing archaea and bacteria in a pollutants' receiving area in Hangzhou Bay[J]. Applied Microbiology and Biotechnology, 2016,100:6035-6045. [38] Palit K, Rath S, Chatterjee S, et al. Microbial diversity and ecological interactions of microorganisms in the mangrove ecosystem:Threats, vulnerability, and adaptations[J]. Environmental Science and Pollution Research, 2022,29(22):32467-32512. [39] Zhou Z Y, Yu M H, Ding G D, et al. Effects of Hedysarum leguminous plants on soil bacterial communities in the Mu Us Desert, northwest China[J]. Ecology and Evolution, 2020,10(20):11423-11439. [40] Nicol G W, Leininger S, Schleper C, et al. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria[J]. Environmental Microbiology, 2008,10(11):2966-2978. [41] Wang X M, Wang S Y, Shi G S, et al. Factors driving the distribution and role of AOA and AOB in Phragmites communis rhizosphere in riparian zone[J]. Journal of Basic Microbiology, 2019,59(4):425-436. [42] Yang W, An S Q, Zhao H, et al. Impacts of Spartina alterniflora invasion on soil organic carbon and nitrogen pools sizes, stability, and turnover in a coastal salt marsh of eastern China[J]. Ecological Engineering, 2016,86:174-182. [43] Wang Y F, Feng Y Y, Gu J D, et al. Seasonal dynamics of ammonia/ammonium-oxidizing prokaryotes in oxic and anoxic wetland sediments of subtropical coastal mangrove[J]. Applied Microbiology and Biotechnology, 2013,97(3):7919-7934. [44] 霍玉珠,王银华,王春萍,等.互花米草入侵对天津滨海湿地土壤可培养细菌和真菌群落组成及多样性的影响[J]. 天津师范大学学报(自然科学版), 2021,41(1):34-41. Huo Y Z, Wang Y H, Wang C P, et al. Effects of Spartina alterniflora invasion on the composition and diversity of culturable soil bacterial and fungal communities in Tianjin coastal wetland[J]. Journal of Tianjin Normal University (Natural Science Edition), 2021,41(1):34-41. [45] Erguder T H, Boon N, Wittebolle L, et al. Environmental factors shaping the ecological niches of ammonia-oxidizing archaea[J]. FEMS Microbiology reviews, 2009,33(5):855-869. [46] Bernhard A E, Donn T, Giblin A E, et al. Loss of diversity of ammonia-oxidizing bacteria correlates with increasing salinity in an estuary system[J]. Environmental Microbiology, 2005,7(9):1289-1297. [47] Francis C A, O'Mullan G D, Ward B B. Diversity of ammonia monooxygenase (amoA) genes across environmental gradients in Chesapeake Bay sediments[J]. Geobiology, 2003,1(2):129-140. [48] Freitag T E, Chang L S, Prosser J I. Changes in the community structure and activity of betaproteobacterial ammonia-oxidizing sediment bacteria along a freshwater-marine gradient[J]. Environmental Microbiology, 2006,8(4):684-696.
