Abstract
Microorganisms are crucial elements of terrestrial ecosystems, which play significant roles in improving soil physicochemical properties, providing plant growth nutrients, degrading toxic and harmful chemicals, and biogeochemical cycling. Variations in the types and quantities of root exudates among different plants greatly alter soil physicochemical properties and result in variations in the diversity, structure, and function of soil microorganisms. Not much is understood about the differences of soil fungi and archaea communities for different plant communities in coastal wetlands, and their response mechanisms to environmental changes. In this study, fungal and archaea communities in soils of Suaeda salsa, Phragmites australis, and Spartina alterniflora in the intertidal habitat of coastal wetlands were selected for research. Soil fungi and archaea were analyzed for diversity, community structure, and function using high throughput ITS and 16S rRNA gene sequencing. The study revealed significant differences in fungi and archaea’s diversity and community structure in the rhizosphere soil of three plant communities. At the same time, there is no significant difference in the functional groups. SOM, TP, AP, MC, EC and SOM, TN, TP, AP, MC, EC are the primary environmental determinants affecting changes in soil fungal and archaeal communities, respectively. Variations in the diversity, community structure, and ecological functions of fungi and archaea can be used as indicators characterizing the impact of external disturbances on the soil environment, providing a theoretical foundation for the effective utilization of soil microbial resources, thereby achieving the goal of environmental protection and health promotion.
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References
Adamczyk, M., Hagedorn, F., Wipf, S., Donhauser, J., Vittoz, P., Rixen, C., Frossard, A., Theurillat, J. P., & Frey, B. (2019). The soil microbiome of Gloria Mountain summits in the Swiss Alps. Frontiers in Microbiology, 10, 1080. https://doi.org/10.3389/fmicb.2019.01080
Bai, R., Wang, J. T., Deng, Y., He, J. Z., Feng, K., & Zhang, L. M. (2017). Microbial community and functional structure significantly varied among distinct types of paddy soils but responded differently along gradients of soil depth layers. Frontiers in Microbiology, 8, 945. https://doi.org/10.3389/fmicb.2017.00945
Baricz, A., Cristea, A., Muntean, V., Teodosiu, G., Andrei, A., Molnár, I., Alexe, M., Rakosy-Tican, E., & Banciu, H. L. (2015). Culturable diversity of aerobic halophilic archaea (Fam. Halobacteriaceae) from hypersaline, meromictic Transylvanian lakes. Extremophiles, 19(2), 525–537. https://doi.org/10.1007/s00792-015-0738-1
Berg, G., & Smalla, K. (2009). Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiology Ecology, 68(1), 1–13. https://doi.org/10.1111/j.1574-6941.2009.00654.x
Carmona, R., Muñoz, R., & Niell, F. X. (2021). Differential nutrient uptake by saltmarsh plants is modified by increasing salinity. Frontiers in Plant Science, 12, 709453. https://doi.org/10.3389/fpls.2021.709453
Chao, A. (1984). Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, 265–270.
Chao, A., & Yang, M. C. (1993). Stopping rules and estimation for recapture debugging with unequal failure rates. Biometrika, 80(1), 193–201. https://doi.org/10.1093/biomet/80.1.193
Chi, Z., Wang, W., Li, H., Wu, H., & Yan, B. (2021). Soil organic matter and salinity as critical factors affecting the bacterial community and function of Phragmites australis-dominated riparian and coastal wetlands. Science of the Total Environment, 762, 143156. https://doi.org/10.1016/j.scitotenv.2020.143156
Craft, C. (2007). Freshwater input structures soil properties, vertical accretion, and nutrient accumulation of Georgia and US tidal marshes. Limnology and Oceanography, 52(3), 1220–1230. https://doi.org/10.4319/lo.2007.52.3.1220
Da Costa, M. S., Santos, H., & Galinski, E. A. (1998). An overview of the role and diversity of compatible solutes in Bacteria and Archaea. Biotechnology of Extremophiles. https://doi.org/10.1007/BFb0102291
Dave, B. P., & Soni, A. (2013). Diversity of halophilic archaea at salt pans around Bhavnagar coast, Gujarat. Proceedings of the National Academy of Sciences, India Section b: Biological Sciences, 83(2), 225–232. https://doi.org/10.1007/s40011-012-0124-z
De Vries, F. T., Griffiths, R. I., Knight, C. G., Nicolitch, O., & Williams, A. (2020). Harnessing rhizosphere microbiomes for drought-resilient crop production. Science, 368(6488), 270–274. https://doi.org/10.1126/science.aaz5192
De Souza Silva, C. M. M., & Fay, E. F. (2012). Effect of salinity on soil microorganisms. Soil Health and Land Use Management, 10, 177–198. https://doi.org/10.5772/28613
Deegan, L. A., Bowen, J. L., Drake, D., Fleeger, J. W., Friedrichs, C. T., Galváalv, T., GaHobbie, J. E., Hopkinson, C., Johnson, D. S., Johnson, J. M., Lemay, L. E., Miller, E., Peterson, B. J., Picard, C., Sheldon, S., Sutherland, M., Vallion, J., & Warren, R. S. (2007). Susceptibility of salt marshes to nutrient enrichment and predator removal. Ecological Applications, 17(sp5), S42–S63. https://doi.org/10.1890/06-0452.1
Deegan, L. A., Johnson, D. S., Warren, R. S., Peterson, B. J., Fleeger, J. W., Fagherazzi, S., & Wollheim, W. M. (2012). Coastal eutrophication as a driver of salt marsh loss. Nature, 490(7420), 388–392. https://doi.org/10.1038/nature11533
Dridi, B., Raoult, D., & Drancourt, M. (2011). Archaea as emerging organisms in complex human microbiomes. Anaerobe, 17(2), 56–63. https://doi.org/10.1016/j.anaerobe.2011.03.001
Douglas, G. M., Maffei, V. J., Zaneveld, J. R., Yurgel, S. N., Brown, J. R., Taylor, C. M., Huttenhower, C., & Langille, M. G. (2020). PICRUSt2 for prediction of metagenome functions. Nature Biotechnology, 38(6), 685–688. https://doi.org/10.1038/s41587-020-0548-6
Donhauser, J., & Frey, B. (2018). Alpine soil microbial ecology in a changing world. FEMS Microbiology Ecology, 94(9), fiy099. https://doi.org/10.1093/femsec/fiy099
Escudero, V., & Mendoza, R. (2005). Seasonal variation of arbuscular mycorrhizal fungi in temperate grasslands along a wide hydrologic gradient. Mycorrhiza, 15(4), 291–299. https://doi.org/10.1007/s00572-004-0332-3
Etesami, H., & Adl, S. M. (2020). Plant growth-promoting rhizobacteria (PGPR) and their action mechanisms in availability of nutrients to plants. Phyto-Microbiome in Stress Regulation. https://doi.org/10.1007/978-981-15-2576-6_9
Fierer, N. (2017). Embracing the unknown: Disentangling the complexities of the soil microbiome. Nature Reviews Microbiology, 15(10), 579–590. https://doi.org/10.1038/nrmicro.2017.87
Garbeva, P., Van Elsas, J. D., & Van Veen, J. A. (2008). Rhizosphere microbial community and its response to plant species and soil history. Plant and Soil, 302, 19–32. https://doi.org/10.1007/s11104-007-9432-0
Goh, C. H., Veliz Vallejos, D. F., Nicotra, A. B., & Mathesius, U. (2013). The impact of beneficial plant-associated microbes on plant phenotypic plasticity. Journal of Chemical Ecology, 39(7), 826–839. https://doi.org/10.1007/s10886-013-0326-8
Guo, J., Du, M., Tian, H., & Wang, B. (2020). Exposure to high salinity during seed development markedly enhances seedling emergence and fitness of the progeny of the extreme halophyte Suaeda salsa. Frontiers in Plant Science, 11, 1291. https://doi.org/10.3389/fpls.2020.01291
Herndl, G. J., Reinthaler, T., Teira, E., van Aken, H., Veth, C., Pernthaler, A., & Pernthaler, J. (2005). Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Applied and Environmental Microbiology, 71(5), 2303–2309. https://doi.org/10.1128/AEM.71.5.2303-2309.2005
Hinsinger, P., Bengough, A. G., Vetterlein, D., & Young, I. M. (2009). Rhizosphere: Biophysics, biogeochemistry and ecological relevance. Plant and Soil, 321, 117–152. https://doi.org/10.1007/s11104-008-9885-9
Huang, L., Bai, J., Wen, X., Zhang, G., Zhang, C., Cui, B., & Liu, X. (2020). Microbial resistance and resilience in response to environmental changes under the higher intensity of human activities than global average level. Global Change Biology, 26, 2377–2389. https://doi.org/10.1111/gcb.14995
Jiao, S., Xu, Y., Zhang, J., & Lu, Y. (2019). Environmental filtering drives distinct continental atlases of soil archaea between dryland and wetland agricultural ecosystems. Microbiome, 7(1), 1–13. https://doi.org/10.1186/s40168-019-0630-9
Kang, E., Li, Y., Zhang, X., Yan, Z., Wu, H., Li, M., Yan, L., Zhang, K., Wang, J. Z., & Kang, X. (2021). Soil pH and nutrients shape the vertical distribution of microbial communities in an alpine wetland. Science of the Total Environment, 774, 145780. https://doi.org/10.1016/j.scitotenv.2021.145780
Li, J., Cui, L., Delgado-Baquerizo, M., Wang, J., Zhu, Y., Wang, R., Li, W., Lei, Y., Zhai, X., Zhao, X., & Singh, B. K. (2022). Fungi drive soil multifunctionality in the coastal salt marsh ecosystem. Science of the Total Environment, 818, 151673. https://doi.org/10.1016/j.scitotenv.2021.151673
Liang, C., & Balser, T. C. (2011). Microbial production of recalcitrant organic matter in global soils: Implications for productivity and climate policy. Nature Reviews Microbiology, 9(1), 75–75. https://doi.org/10.1038/nrmicro2386-c1
Liu, C., Li, X., Mansoldo, F. R., An, J., Kou, Y., Zhang, X., Wang, J., Zeng, J., Vermelho, A. B., & Yao, M. (2022). Microbial habitat specificity largely affects microbial co-occurrence patterns and functional profiles in wetland soils. Geoderma, 418, 115866. https://doi.org/10.1016/j.geoderma.2022.115866
Liu, F., Mo, X., Kong, W., & Song, Y. (2020). Soil bacterial diversity, structure, and function of Suaeda salsa in rhizosphere and non-rhizosphere soils in various habitats in the Yellow River Delta China. Science of the Total Environment, 740, 140144. https://doi.org/10.1016/j.scitotenv.2020.140144
Mo, X., Song, Y., Chen, F., You, C., Li, D., & Liu, F. (2023). Replacement of plant communities altered soil bacterial diversity and structure rather than the function in similar habitats of the Yellow River Delta. China. Ecological Indicators, 146, 109793. https://doi.org/10.1016/j.ecolind.2022.109793
Miki, T., Ushio, M., Fukui, S., & Kondoh, M. (2010). Functional diversity of microbial decomposers facilitates plant coexistence in a plant-microbe-soil feedback model. Proceedings of the National Academy of Sciences, 107(32), 14251–14256. https://doi.org/10.1073/pnas.0914281107
Murray, N. J., Phinn, S. R., DeWitt, M., Ferrari, R., Johnston, R., Lyons, M. B., Clinton, N., Thau, D., & Fuller, R. A. (2019). The global distribution and trajectory of tidal flats. Nature, 565, 222–225. https://doi.org/10.1038/s41586-018-0805-8
Ndayegamiye, A., & Cote, D. (1989). Effect of long-term pig slurry and solid cattle manure application on soil chemical and biological properties. Canadian Journal of Soil Science, 69(1), 39–47. https://doi.org/10.4141/cjss89-005
Nguyen, N., Song, Z., Bates, S. T., Branco, S., Tedersoo, L., Menke, Jon, Schilling, J. S., & Kennedy, P. G. (2016). FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology, 20, 241–248. https://doi.org/10.1016/j.funeco.2015.06.006
Ochsenreiter, T., Pfeifer, F., & Schleper, C. (2002). Diversity of Archaea in hypersaline environments characterized by molecular-phylogenetic and cultivation studies. Extremophiles, 6(4), 267–274. https://doi.org/10.1007/s00792-001-0253-4
Overmann, J., & Lepleux, C. (2016). Marine bacteria and archaea: diversity, adaptations, and culturability. The Marine Microbiome: an Untapped Source of Biodiversity and Biotechnological Potential. https://doi.org/10.1007/978-3-319-33000-6_2
Oren, A. (2014). Halophilic archaea on Earth and in space: growth and survival under extreme conditions. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, 372, 20140194. https://doi.org/10.1098/rsta.2014.0194
Oueriaghli, N., Béjar, V., Quesada, E., & Martínez-Checa, F. (2013). Molecular ecology techniques reveal both spatial and temporal variations in the diversity of archaeal communities within the athalassohaline environment of Rambla Salada Spain. Microbial Ecology, 66(2), 297–311. https://doi.org/10.1007/s00248-013-0176-5
Prober, S. M., Leff, J. W., Bates, S. T., Borer, E. T., Jennifer Firn, W., Harpole, S., Lind, E. M., Seabloom, E. W., Adler, P. B., Bakker, J. D., Cleland, E. E., DeCrappeo, N. M., DeLorenze, E., Hagenah, N., Hautier, Y., Hofmockel, K. S., Kirkman, K. P., Knops, J. M. H., La Pierre, K. J., … Fierer, N. (2015). Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecology Letters, 18(1), 85–95. https://doi.org/10.1111/ele.12381
Prodan, A., Tremaroli, V., Brolin, H., Zwinderman, A. H., Nieuwdorp, M., & Levin, E. (2020). Comparing bioinformatic pipelines for microbial 16S rRNA amplicon sequencing. PLoS ONE, 15(1), e0227434. https://doi.org/10.1371/journal.pone.0227434
Qian, H., Ju, P., Zhang, D., Ma, L., Hu, Y., Li, Z., Huang, L., Lou, Y., & Du, C. (2019). Effect of dissolved oxygen concentration on the microbiologically influenced corrosion of Q235 carbon steel by halophilic archaeon Natronorubrum tibetense. Frontiers in Microbiology, 10, 844. https://doi.org/10.3389/fmicb.2019.00844
Qin, S., Yeboah, S., Xu, X., Liu, Y., & Yu, B. (2017). Analysis on fungal diversity in rhizosphere soil of continuous cropping potato subjected to different furrow-ridge mulching managements. Frontiers in Microbiology, 8, 845. https://doi.org/10.3389/fmicb.2017.00845
Richter, I., Herbold, C. W., Lee, C. K., McDonald, I. R., Barrett, J. E., & Cary, S. C. (2014). Influence of soil properties on archaeal diversity and distribution in the McMurdo Dry Valleys. Antarctica. FEMS Microbiology Ecology, 89(2), 347–359. https://doi.org/10.1111/1574-6941.12322
Riley, D., & Barber, S. A. (1971). Effect of ammonium and nitrate fertilization on phosphorus uptake as related to root-induced pH changes at the root-soil interface. Soil Science Society of America Journal, 35(2), 301–306. https://doi.org/10.2136/sssaj1971.03615995003500020035x
Rodriguez, P. A., Rothballer, M., Chowdhury, S. P., Nussbaumer, T., Gutjahr, C., & Falter-Braun, P. (2019). Systems biology of plant-microbiome interactions. Molecular Plant, 12(6), 804–821. https://doi.org/10.1016/j.molp.2019.05.006
Sharma, S. K., Ramesh, A., Sharma, M. P., Joshi, O. P., Govaerts, B., Steenwerth, K. L., & Karlen, D. L. (2011). Microbial community structure and diversity as indicators for evaluating soil quality. Biodiversity, Biofuels, Agroforestry and Conservation Agriculture. https://doi.org/10.1007/978-90-481-9513-8_11
Shannon, C. E. (1948). A mathematical theory of communication. The Bell System Technical Journal, 27(3), 379–423. https://doi.org/10.1002/j.1538-7305.1948.tb01338.x
Shi, H., Gao, W., Zheng, Y., Yang, L., Han, B., Zhang, Y., & Zheng, L. (2023). Distribution and abundance of oil-degrading bacteria in seawater of the Yellow Sea and Bohai Sea China. Science of the Total Environment, 902, 166038. https://doi.org/10.1016/j.scitotenv.2023.166038
Tedersoo, L., Bahram, M., Toots, M., Di’edhiou, A. G., Henkel, T. W., Kjoller, R., Morris, M. H., Nara, K., Nouhra, E., Peay, K. G., Polme, S., Ryberg, M., Smith, M. E., & Koljalg, U. (2012). Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Molecular Ecology, 21, 4160–4170. https://doi.org/10.1111/j.1365-294X.2012.05602.x
Wang, X., Sun, R., Tian, Y., Guo, K., Sun, H., Liu, X., Chu, H., & Liu, B. (2020). Long-term phytoremediation of coastal saline soil reveals plant species-specific patterns of microbial community recruitment. Msystems, 5(2), e00741-e819. https://doi.org/10.1128/msystems.00741-19
Xie, L. N., Ge, Z. M., Li, Y. L., Li, S. H., Tan, L. S., & Li, X. Z. (2020). Effects of waterlogging and increased salinity on microbial communities and extracellular enzyme activity in native and exotic marsh vegetation soils. Soil Science Society of America Journal, 84(1), 82–98. https://doi.org/10.1002/saj2.20006
Yang, W., Cai, A. D., Wang, J. S., Luo, Y. Q., Cheng, X. L., & An, S. Q. (2020). Exotic Spartina alterniflora Loisel. invasion significantly shifts soil bacterial communities with the successional gradient of saltmarsh in eastern China. Plant and Soil, 449, 97–115. https://doi.org/10.1007/s11104-020-04470-y
Zafrilla, B., MartBnez-Espinosa, R. M., Alonso, M. A., & Bonete, M. J. (2010). Biodiversity of Archaea and floral of two inland saltern ecosystems in the Alto Vinalopó Valley, Spain. Saline Systems, 6, 1–12. https://doi.org/10.1186/1746-1448-6-10
Zhang, K., Shi, Y., Cui, X., Yue, P., Li, K., Liu, X., Tripathi, B. M., & Chu, H. (2019). Salinity is a key determinant for soil microbial communities in a desert ecosystem. Msystems, 4(1), e00225. https://doi.org/10.1128/msystems.00225-18
Zhang, Y., Li, Y., Wang, L., Tang, Y., Chen, J., Hu, Y., Fu, X., & Le, Y. (2013). Soil microbiological variability under different successional stages of the Chongming Dongtan wetland and its effect on soil organic carbon storage. Ecological Engineering, 52, 308–315. https://doi.org/10.1016/j.ecoleng.2012.10.002
Zhao, F. Z., Bai, L., Wang, J. Y., Deng, J., Ren, C. J., Han, X. H., Yang, G. H., & Wang, J. (2019). Change in soil bacterial community during secondary succession depend on plant and soil characteristics. CATENA, 173, 246–252. https://doi.org/10.1016/j.catena.2018.10.024
Zhou, J. Z., Deng, Y., Shen, L. N., Wen, C. Q., Yan, Q. Y., Ning, D. L., Qin, Y. J., Xue, K., Wu, L. Y., He, Z. L., Voordeckers, J. W., Van Nostrand, J. D., Buzzard, V., Michaletz, S. T., Enquist, B. J., Weiser, M. D., Kaspari, M., Waide, R., Yang, Y. F., & Brown, J. H. (2016). Temperature mediates continental-scale diversity of microbes in forest soils. Nature Communications, 7(1), 12083. https://doi.org/10.1038/ncomms12083
Zou, Q., Lin, G., Jiang, X., Liu, X., & Zeng, X. (2020). Sequence clustering in bioinformatics: An empirical study. Briefings in Bioinformatics, 21(1), 1–10. https://doi.org/10.1093/bib/bby090
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This work was supported by the Fundamental Research Funds for Central Public Welfare Scientific Research Institutes of China (2022YSKY-41).
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All authors contributed to the study's conception and design. Material preparation, data collection and analysis were performed by XG, SW and WK. Software acquisition was performed by GL, LZ and XY. Funding acquisition was performed by WK. The first draft of the manuscript was written by XG, SW and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Gao, X., Wang, S., Kong, W. et al. Floristic changes and environmental drivers of soil fungi and archaea in different salt-tolerant plant communities in the intertidal habitat of coastal wetlands. Environ Geochem Health 46, 167 (2024). https://doi.org/10.1007/s10653-024-01951-2
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DOI: https://doi.org/10.1007/s10653-024-01951-2