Volume 41 Issue 8
Aug.  2022
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Wu Qu, Michael Vicent Shija, Jie Wu, Min Jin, Jianxin Wang, Runying Zeng, Zhuhua Chan. Particle size shapes the prokaryotic microbial communities in mangrove sediments: A case study of Sanya, China[J]. Acta Oceanologica Sinica, 2022, 41(8): 120-128. doi: 10.1007/s13131-021-1915-y
Citation: Wu Qu, Michael Vicent Shija, Jie Wu, Min Jin, Jianxin Wang, Runying Zeng, Zhuhua Chan. Particle size shapes the prokaryotic microbial communities in mangrove sediments: A case study of Sanya, China[J]. Acta Oceanologica Sinica, 2022, 41(8): 120-128. doi: 10.1007/s13131-021-1915-y

Particle size shapes the prokaryotic microbial communities in mangrove sediments: A case study of Sanya, China

doi: 10.1007/s13131-021-1915-y
Funds:  Natural Science Foundation of Zhejiang under contract No. LQ22D060004; the Scientific Research Foundation of Third Institute of Oceanography, Ministry of Natural Resources under contract No. 2019013; the Science and Technology Program of Zhoushan under contract No. 2019C21011.
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  • Corresponding author: E-mail: chan@tio.org.cn
  • Received Date: 2021-04-29
  • Accepted Date: 2021-07-13
  • Available Online: 2022-04-27
  • Publish Date: 2022-08-15
  • The prokaryotic microbial communities in the sediments play crucial roles in the ecological functions of mangrove ecosystems. Therefore, the environmental factors that affect the structures of these prokaryotic microbial communities could indirectly participate in the regulation of mangrove functions, which is of great value for mangrove studies. The particle size (PS) of soils is recently demonstrated as a key environmental factor for shaping the microbial communities; however, this hypothesis has rarely been tested for mangrove environments. A case study of three tropical mangroves from Sanya, China was performed in this work to assess the influence of PS on the prokaryotic microbial community structures of bacteria, archaea, diazotrophs, and denitrifiers in the sediments. Results showed the variability in the spatial scale and the stability in the temporal scale for the prokaryotic communities, indicating that the tropical mangrove sediments could be a versatile but stable environment. Among the collected environmental factors, PS, salinity, and humidity had the greatest impacts, and PS mostly affected the structures of these prokaryotic communities based on its highest R2 values of canonical correspondence analysis, Mental test, and linear fitting (p≤0.05). Furthermore, PS was positively correlated with the diversity and abundance of diazotrophic communities and negatively correlated with the abundances of methanogenic communities including Methanobacteriaceae, Methanospirillaceae, Methanoregulaceae, and Methanosaetaceae. Former studies show the increasing trend of PS caused by the rise of sea level and the intensification of human activities. Therefore, our findings indicate that PS could be a potential intermediate that links climate change and human activities with the possible ecological function migration of mangroves; meanwhile, the increase of PS could in turn release the stress of these environmental changes by increasing the abundance and diversity of the diazotrophic community and decreasing the abundances of methanogens.
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  • [1]
    Alongi D M, Boto K G, Robertson A I. 1992. Nitrogen and phosphorus cycles. In: Robertson A I, Alongi D M, eds. Tropical Mangrove Ecosystems, Volume 41. Washington: American Geophysical Union
    [2]
    Alongi D M, Murdiyarso D, Fourqurean J W, et al. 2016. Indonesia’s blue carbon: a globally significant and vulnerable sink for seagrass and mangrove carbon. Wetlands Ecology and Management, 24(1): 3–13. doi: 10.1007/s11273-015-9446-y
    [3]
    Basak P, Majumder N S, Nag S, et al. 2015. Spatiotemporal analysis of bacterial diversity in sediments of Sundarbans using parallel 16S rRNA gene tag sequencing. Microbial ecology, 69(3): 500–511. doi: 10.1007/s00248-014-0498-y
    [4]
    Behera P, Mohapatra M, Kim J Y, et al. 2019. Spatial and temporal heterogeneity in the structure and function of sediment bacterial communities of a tropical mangrove forest. Environmental Science and Pollution Research, 26(4): 3893–3908. doi: 10.1007/s11356-018-3927-5
    [5]
    Boto K G, Wellington J T. 1983. Phosphorus and nitrogen nutritional status of a northern Australian mangrove forest. Marine Ecology-Progress Series, 11: 63–69. doi: 10.3354/meps011063
    [6]
    Chambers L G, Guevara R, Boyer J N, et al. 2016. Effects of salinity and inundation on microbial community structure and function in a mangrove peat soil. Wetlands, 36(2): 361–371. doi: 10.1007/s13157-016-0745-8
    [7]
    Chen Junhui, He Feng, Zhang Xuhui, et al. 2014. Heavy metal pollution decreases microbial abundance, diversity and activity within particle-size fractions of a paddy soil. FEMS Microbiology Ecology, 87(1): 164–181. doi: 10.1111/1574-6941.12212
    [8]
    Curtis T P, Sloan W T. 2004. Prokaryotic diversity and its limits: microbial community structure in nature and implications for microbial ecology. Current Opinion in Microbiology, 7(3): 221–226. doi: 10.1016/j.mib.2004.04.010
    [9]
    Dong Lianhui, Meng Ying, Wang Jing, et al. 2014. Erratum to: evaluation of droplet digital PCR for characterizing plasmid reference material used for quantifying ammonia oxidizers and denitrifiers. Analytical and Bioanalytical Chemistry, 406(20): 5065. doi: 10.1007/s00216-014-7973-7
    [10]
    Fan Wenguang, Tang Yaru, Qu Yi, et al. 2014. Infant formula supplemented with low protein and high carbohydrate alters the intestinal microbiota in neonatal SD rats. BMC Microbiology, 14: 279. doi: 10.1186/s12866-014-0279-2
    [11]
    Feller I C, McKee K L, Whigham D F, et al. 2003a. Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry, 62(2): 145–175. doi: 10.1023/A:1021166010892
    [12]
    Feller I C, Whigham D F, McKee K L, et al. 2003b. Nitrogen limitation of growth and nutrient dynamics in a disturbed mangrove forest, Indian River Lagoon, Florida. Oecologia, 134(3): 405–414. doi: 10.1007/s00442-002-1117-z
    [13]
    Flores-Mireles A L, Winans S C, Holguin G. 2007. Molecular characterization of diazotrophic and denitrifying bacteria associated with mangrove roots. Applied and Environmental Microbiology, 73(22): 7308–7321. doi: 10.1128/AEM.01892-06
    [14]
    Gangi A F. 1985. Permeability of unconsolidated sands and porous rocks. Journal of Geophysical Research: Solid Earth, 90(B4): 3099–3104. doi: 10.1029/JB090iB04p03099
    [15]
    Guo Zixiao, Li Xinnian, He Ziwen, et al. 2018. Extremely low genetic diversity across mangrove taxa reflects past sea level changes and hints at poor future responses. Global Change Biology, 24(4): 1741–1748. doi: 10.1111/gcb.13968
    [16]
    Haines S R, Bope A, Horack J M, et al. 2019. Quantitative evaluation of bioaerosols in different particle size fractions in dust collected on the International Space Station (ISS). Applied Microbiology and Biotechnology, 103(18): 7767–7782. doi: 10.1007/s00253-019-10053-4
    [17]
    Hinsley A. 2011. World Atlas of Mangroves by Mark Spalding, Mami Kainuma and Lorna Collins (2010), 336 pp., Earthscan, London, UK. ISBN 9781844076574 (hbk), GBP 65.00. Oryx, 45(2): 306. doi: 10.1017/S0030605311000585
    [18]
    Imachi H, Sakai S. 2015. Methanoregulaceae. In: Bergey’s Manual of Systematics of Archaea and Bacteria. Hoboken, New Jersey: Wiley, 1–4
    [19]
    Jin Min, Guo Xun, Zhang Rui, et al. 2019. Diversities and potential biogeochemical impacts of mangrove soil viruses. Microbiome, 7(1): 58. doi: 10.1186/s40168-019-0675-9
    [20]
    Kandeler E, Stemmer M, Klimanek E M. 1999. Response of soil microbial biomass, urease and xylanase within particle size fractions to long-term soil management. Soil Biology and Biochemistry, 31(2): 261–273. doi: 10.1016/S0038-0717(98)00115-1
    [21]
    Kandeler E, Tscherko D, Bruce K D, et al. 2000. Structure and function of the soil microbial community in microhabitats of a heavy metal polluted soil. Biology and Fertility of Soils, 32(5): 390–400. doi: 10.1007/s003740000268
    [22]
    Karakashev D, Batstone D J, Trably E, et al. 2006. Acetate oxidation is the dominant methanogenic pathway from acetate in the absence of Methanosaetaceae. Applied and Environmental Microbiology, 72(7): 5138–5141. doi: 10.1128/AEM.00489-06
    [23]
    Li Mingyue, Fang Anqi, Yu Xiaoli, et al. 2021. Microbially-driven sulfur cycling microbial communities in different mangrove sediments. Chemosphere, 273: 128597. doi: 10.1016/j.chemosphere.2020.128597
    [24]
    Lin Xiaolan, Hetharua B, Lin Lian, et al. 2019. Mangrove sediment microbiome: adaptive microbial assemblages and their routed biogeochemical processes in Yunxiao Mangrove National Nature Reserve, China. Microbial Ecology, 78(1): 57–69. doi: 10.1007/s00248-018-1261-6
    [25]
    Liu Yalong, Dong Y, Wang P, et al. 2019. Distribution of methane production and methanogenic archaeal community structure across soil particle size fractions along a rice chronosequence. Journal of Soil and Water Conservation, 74(3): 235–246. doi: 10.2489/jswc.74.3.235
    [26]
    Liu Shuai, Ren Hongxing, Shen Lidong, et al. 2015. pH levels drive bacterial community structure in sediments of the Qiantang River as determined by 454 pyrosequencing. Frontiers in Microbiology, 6: 285
    [27]
    Liu Min, Yu Zheng, Yu Xiaoqing, et al. 2017. Invasion by cordgrass increases microbial diversity and alters community composition in a mangrove nature reserve. Frontiers in Microbiology, 8: 2503. doi: 10.3389/fmicb.2017.02503
    [28]
    Lovelock C E, Feller I C, Ball M C, et al. 2006. Differences in plant function in phosphorus-and nitrogen-limited mangrove ecosystems. New Phytologist, 172(3): 514–522. doi: 10.1111/j.1469-8137.2006.01851.x
    [29]
    Luo Ling, Gu Jidong. 2018. Nutrient limitation status in a subtropical mangrove ecosystem revealed by analysis of enzymatic stoichiometry and microbial abundance for sediment carbon cycling. International Biodeterioration & Biodegradation, 128: 3–10
    [30]
    Luo Ling, Zhou Zhichao, Gu Jidong. 2015. Distribution, diversity and abundance of bacterial laccase-like genes in different particle size fractions of sediments in a subtropical mangrove ecosystem. Ecotoxicology, 24(7): 1508–1516
    [31]
    Mao Longjiang, Zhang Yongzhan, Zhang Zhenke, et al. 2007. Characteristics of sedimentary environments in Sanya Bay of Hainan Island. Marine Geology & Quaternary Geology, 27(4): 17–22
    [32]
    Oades J M. 1984. Soil organic matter and structural stability: mechanisms and implications for management. Plant and Soil, 76(1−3): 319–337. doi: 10.1007/BF02205590
    [33]
    Oren A. 2014. The family Methanobacteriaceae. In: Rosenberg E, DeLong E F, Lory S, et al., eds. The Prokaryotes. Berlin, Heidelberg: Springer,165–193
    [34]
    Postma J, van Veen J A. 1990. Habitable pore space and survival of Rhizobium leguminosarum biovartrifolii introduced into soil. Microbial Ecology, 19(2): 149–161. doi: 10.1007/BF02012096
    [35]
    Punwong P, Sritrairat S, Selby K, et al. 2018. An 800 year record of mangrove dynamics and human activities in the upper Gulf of Thailand. Vegetation History and Archaeobotany, 27(4): 535–549. doi: 10.1007/s00334-017-0651-x
    [36]
    Qiu Yaowen, Qiu Hanlin, Zhang Gan, et al. 2019. Bioaccumulation and cycling of organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs) in three mangrove reserves of south China. Chemosphere, 217: 195–203. doi: 10.1016/j.chemosphere.2018.10.188
    [37]
    Rösch C, Mergel A, Bothe H. 2002. Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Applied and Environmental Microbiology, 68(8): 3818–3829. doi: 10.1128/AEM.68.8.3818-3829.2002
    [38]
    Ruitenbeek H J. 1995. Functions of nature: evaluation of nature in environmental planning, management and decision making: Rudolph S. de Groot. Wolters-Noordhoff, Amsterdam, 1992.315 pp. ISBN 90-01-35594-3. Ecological Economics, 14(3): 211–213. doi: 10.1016/0921-8009(95)90061-6
    [39]
    Sanders C J, Smoak J M, Waters M N, et al. 2012. Organic matter content and particle size modifications in mangrove sediments as responses to sea level rise. Marine Environmental Research, 77: 150–155. doi: 10.1016/j.marenvres.2012.02.004
    [40]
    Sessitsch A, Weilharter A, Gerzabek M H, et al. 2001. Microbial population structures in soil particle size fractions of a long-term fertilizer field experiment. Applied and Environmental Microbiology, 67(9): 4215–4224. doi: 10.1128/AEM.67.9.4215-4224.2001
    [41]
    Stemmer M, Gerzabek M H, Kandeler E. 1998a. Invertase and xylanase activity of bulk soil and particle-size fractions during maize straw decomposition. Soil Biology and Biochemistry, 31(1): 9–18. doi: 10.1016/S0038-0717(98)00083-2
    [42]
    Stemmer M, Gerzabek M H, Kandeler E. 1998b. Organic matter and enzyme activity in particle-size fractions of soils obtained after low-energy sonication. Soil Biology and Biochemistry, 30(1): 9–17. doi: 10.1016/S0038-0717(97)00093-X
    [43]
    Sunagawa S, Acinas S G, Bork P, et al. 2020. Tara Oceans: towards global ocean ecosystems biology. Nature Reviews Microbiology, 18(8): 428–445. doi: 10.1038/s41579-020-0364-5
    [44]
    Tue N T, Ngoc N T, Quy T D, et al. 2012. A cross-system analysis of sedimentary organic carbon in the mangrove ecosystems of Xuan Thuy National Park, Vietnam. Journal of Sea Research, 67(1): 69–76. doi: 10.1016/j.seares.2011.10.006
    [45]
    Vanegas J, Muñoz-García A, Pérez-Parra K A, et al. 2019. Effect of salinity on fungal diversity in the rhizosphere of the halophyte Avicennia germinans from a semi-arid mangrove. Fungal Ecology, 42: 100855. doi: 10.1016/j.funeco.2019.07.009
    [46]
    Wang Haitao, Gilbert J A, Zhu Yongguan, et al. 2018. Salinity is a key factor driving the nitrogen cycling in the mangrove sediment. Science of the Total Environment, 631–632: 1342–1349
    [47]
    Xia Xinghui, Li Zhihuang, Zhang Sibo, et al. 2019. Occurrence of anammox on suspended sediment (SPS) in oxic river water: effect of the SPS particle size. Chemosphere, 235: 40–48. doi: 10.1016/j.chemosphere.2019.06.161
    [48]
    Yasin N H M, Maeda T, Hu Anyi, et al. 2015. CO2 sequestration by methanogens in activated sludge for methane production. Applied Energy, 142: 426–434. doi: 10.1016/j.apenergy.2014.12.069
    [49]
    Zhalnina K, Dias R, de Quadros P D, et al. 2015. Soil pH determines microbial diversity and composition in the park grass experiment. Microbial Ecology, 69(2): 395–406. doi: 10.1007/s00248-014-0530-2
    [50]
    Zhang Yanying, Yang Qingsong, Ling Juan, et al. 2017. Diversity and structure of diazotrophic communities in mangrove rhizosphere, revealed by high-throughput sequencing. Frontiers in Microbiology, 8: 2032. doi: 10.3389/fmicb.2017.02032
    [51]
    Zhang Pingjiu, Zheng Jufeng, Pan Genxing, et al. 2007. Changes in microbial community structure and function within particle size fractions of a paddy soil under different long-term fertilization treatments from the Tai Lake region, China. Colloids and Surfaces B: Biointerfaces, 58(2): 264–270. doi: 10.1016/j.colsurfb.2007.03.018
    [52]
    Zhou Zhichao, Meng Han, Liu Yang, et al. 2017. Stratified bacterial and archaeal community in mangrove and intertidal wetland mudflats revealed by high throughput 16S rRNA gene sequencing. Frontiers in Microbiology, 8: 2148. doi: 10.3389/fmicb.2017.02148
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