Effects of tourism development on ecological network and function of sediment microbial communities in the urban wetland park

Binhao Wang , Kaiming Hu , Lin Chen , Wei Zhang , Congcong Zhang , Wenbing Li , Hangjun Zhang

Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (4) : 240249

PDF (2717KB)
Soil Ecology Letters ›› 2024, Vol. 6 ›› Issue (4) : 240249 DOI: 10.1007/s42832-024-0249-z
RESEARCH ARTICLE

Effects of tourism development on ecological network and function of sediment microbial communities in the urban wetland park

Author information +
History +
PDF (2717KB)

Abstract

● Tourism development influenced the ecological network of microbial communities.

● Regulating mechanism of intra- and inter-domain networks was clarified.

● Macrophyte coverage reduces microbial network complexity and stability.

● Landscaping may promote nitrogen and phosphorus cycle in wetland watershed.

Numerous urban wetland parks have been established, yet the understanding of microbial interactions in response to tourism development is still limited. This study aims to elucidate the impact of tourism development on the complexity and stability of molecular ecological networks within the microbial communities of wetland sediments. Through an analysis of sediments properties, microorganism intra- and inter-domain co-occurrence characteristics in three different wetland functional areas (conservation, landscaping, and recreation areas), we found that tourism development influenced sediment physicochemical properties. These changes regulated the diversity and ecological networks of archaeal and bacterial communities. Specifically, areas with landscaping (LA) exhibited reduced network connectivity and robustness, suggesting that macrophyte coverage diminishes the complexity and stability of microbial communities in wetland parks. Notably, the transition from conservation areas (CA) to LA strengthened the correlations between microbial network modules and sediment total nitrogen (TN) and total phosphorus (TP), potentially enhancing the nitrogenand phosphorus cycles in wetlands. Structural equation modeling analysisrevealed that both abiotic factors (TC, TP, TN, K, Mg, pH) and biotic factors (archaeal and bacterial α-diversity) can influence interdomain network complexity, accounting for 42% of the variation. Among these factors, sediment TN exerted the largest positive effect on network complexity (37.9%), while Mg had the most negative impact (59.8%). This study provides valuable insights for ecological assessments of urban wetlands and can inform strategies for effective wetland ecosystem management.

Graphical abstract

Keywords

urban wetlands / tourism development / microbial communities / interdomain interactions / network complexity

Cite this article

Download citation ▾
Binhao Wang, Kaiming Hu, Lin Chen, Wei Zhang, Congcong Zhang, Wenbing Li, Hangjun Zhang. Effects of tourism development on ecological network and function of sediment microbial communities in the urban wetland park. Soil Ecology Letters, 2024, 6(4): 240249 DOI:10.1007/s42832-024-0249-z

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Arif, M., Behzad, H.M., Tahir, M., Li, C.X., 2022. Nature-based tourism influences ecosystem functioning along waterways: Implications for conservation and management. Science of the Total Environment842, 156935.

[2]

Arsić, S., Nikolić, D., Mihajlović, I., Fedajev, A., Živković, Ž., 2018. A new approach within ANP-SWOT framework for prioritization of ecosystem management and case study of National Park Djerdap, Serbia. Ecological Economics146, 85–95.

[3]

Banerjee, S., Schlaeppi, K., Van Der Heijden, M.G.A., 2018. Keystone taxa as drivers of microbiome structure and functioning. Nature Reviews Microbiology16, 567–576.

[4]

Banerjee, S., Walder, F., Büchi, L., Meyer, M., Held, A.Y., Gattinger, A., Keller, T., Charles, R., Van Der Heijden, M.G.A., 2019. Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. The ISME Journal13, 1722–1736.

[5]

Boetius, A., 2019. Global change microbiology-big questions about small life for our future. Nature Reviews Microbiology17, 331–332.

[6]

Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., Holmes, S.P., 2016. DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods13, 581–583.

[7]

Chatterjee, K., Bandyopadhyay, A., Ghosh, A., Kar, S., 2015. Assessment of environmental factors causing wetland degradation, using Fuzzy Analytic Network Process: A case study on Keoladeo National Park, India. Ecological Modelling316, 1–13.

[8]

Costanza, R., d'Arge, R., De Groot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K., Naeem, S., O'neill, R.V., Paruelo, J., Raskin, R.G., Sutton, P., Van Den Belt, M., 1997. The value of the world's ecosystem services and natural capital. Nature387, 253–260.

[9]

Coux, C., Rader, R., Bartomeus, I., Tylianakis, J.M., 2016. Linking species functional roles to their network roles. Ecology Letters19, 762–770.

[10]

De Vries, F.T., Griffiths, R.I., Bailey, M., Craig, H., Girlanda, M., Gweon, H.S., Hallin, S., Kaisermann, A., Keith, A.M., Kretzschmar, M., Lemanceau, P., Lumini, E., Mason, K.E., Oliver, A., Ostle, N., Prosser, J.I., Thion, C., Thomson, B., Bardgett, R.D., 2018. Soil bacterial networks are less stable under drought than fungal networks. Nature Communications9, 303.

[11]

Delgado-Baquerizo, M., Reith, F., Dennis, P.G., Hamonts, K., Powell, J.R., Young, A., Singh, B.K., Bissett, A., 2018. Ecological drivers of soil microbial diversity and soil biological networks in the Southern Hemisphere. Ecology99, 583–596.

[12]

Deng, Y., Jiang, Y.H., Yang, Y.F., He, Z.L., Luo, F., Zhou, J.Z., 2012. Molecular ecological network analyses. BMC Bioinformatics13, 113.

[13]

Faust, K., Raes, J., 2012. Microbial interactions: from networks to models. Nature Reviews Microbiology10, 538–550.

[14]

Feng, K., Zhang, Y.G., He, Z.L., Ning, D.L., Deng, Y., 2019. Interdomain ecological networks between plants and microbes. Molecular Ecology Resources19, 1565–1577.

[15]

Fu, G.P., Wu, J.F., Han, J.Y., Zhao, L., Chan, G., Leong, K., 2020. Effects of substrate type on denitrification efficiency and microbial community structure in constructed wetlands. Bioresource Technology307, 123222.

[16]

Fuhrman, J.A., 2009. Microbial community structure and its functional implications. Nature459, 193–199.

[17]

Guo, Y.P., Song, B., Li, A.Q., Wu, Q.L., Huang, H.L., Li, N., Yang, Y., Adams, J.M., Yang, L., 2022. Higher pH is associated with enhanced co-occurrence network complexity, stability and nutrient cycling functions in the rice rhizosphere microbiome. Environmental Microbiology24, 6200–6219.

[18]

Haase, P., Tonkin, J.D., Stoll, S., Burkhard, B., Frenzel, M., Geijzendorffer, I.R., Häuser, C., Klotz, S., Kühn, I., McDowell, W.H., Mirtl, M., Müller, F., Musche, M., Penner, J., Zacharias, S., Schmeller, D.S., 2018. The next generation of site-based long-term ecological monitoring: Linking essential biodiversity variables and ecosystem integrity. Science of the Total Environment 613–614, 613–614

[19]

Heilmayr, R., 2014. Conservation through intensification? The effects of plantations on natural forests.. Ecological Economics105, 204–210.

[20]

Ji, M.K., Williams, T.J., Montgomery, K., Wong, H.L., Zaugg, J., Berengut, J.F., Bissett, A., Chuvochina, M., Hugenholtz, P., Ferrari, B.C., 2021. Candidatus eremiobacterota, a metabolically and phylogenetically diverse terrestrial phylum with acid-tolerant adaptations. The ISME Journal15, 2692–2707.

[21]

Kiersztyn, B., Chróst, R., Kaliński, T., Siuda, W., Bukowska, A., Kowalczyk, G., Grabowska, K., 2019. Structural and functional microbial diversity along a eutrophication gradient of interconnected lakes undergoing anthropopressure. Scientific Reports9, 11144.

[22]

Kuypers, M.M.M., Marchant, H.K., Kartal, B., 2018. The microbial nitrogen-cycling network. Nature Reviews Microbiology16, 263–276.

[23]

Li, C., Hambright, K.D., Bowen, H.G., Trammell, M.A., Grossart, H.P., Burford, M.A., Hamilton, D.P., Jiang, H.L., Latour, D., Meyer, E.I., Padisák, J., Zamor, R.M., Krumholz, L.R., 2021. Global co-occurrence of methanogenic archaea and methanotrophic bacteria in Microcystis aggregates. Environmental Microbiology23, 6503–6519.

[24]

Li, H.J., Chang, J.L., Liu, P.F., Fu, L., Ding, D.W., Lu, Y.H., 2015. Direct interspecies electron transfer accelerates syntrophic oxidation of butyrate in paddy soil enrichments. Environmental Microbiology17, 1533–1547.

[25]

Li, Q.J., Dai, M.Q., Luo, F., 2022. Influence of tourism disturbance on soil microbial community structure in Dawei Mountain national forest park. Sustainability14, 1162.

[26]

Louca, S., Polz, M.F., Mazel, F., Albright, M.B.N., Huber, J.A., O’Connor, M.I., Ackermann, M., Hahn, A.S., Srivastava, D.S., Crowe, S.A., Doebeli, M., Parfrey, L.W., 2018. Function and functional redundancy in microbial systems. Nature Ecology & Evolution2, 936–943.

[27]

Mamet, S.D., Lamb, E.G., Piper, C.L., Winsley, T., Siciliano, S.D., 2017. Archaea and bacteria mediate the effects of native species root loss on fungi during plant invasion. The ISME Journal11, 1261–1275.

[28]

Mamet, S.D., Redlick, E., Brabant, M., Lamb, E.G., Helgason, B.L., Stanley, K., Siciliano, S.D., 2019. Structural equation modeling of a winnowed soil microbiome identifies how invasive plants re-structure microbial networks. The ISME Journal13, 1988–1996.

[29]

Mandakovic, D., Rojas, C., Maldonado, J., Latorre, M., Travisany, D., Delage, E., Bihouée, A., Jean, G., Díaz, F.P., Fernández-Gómez, B., Cabrera, P., Gaete, A., Latorre, C., Gutiérrez, R.A., Maass, A., Cambiazo, V., Navarrete, S.A., Eveillard, D., González, M., 2018. Structure and co-occurrence patterns in microbial communities under acute environmental stress reveal ecological factors fostering resilience. Scientific Reports8, 5875.

[30]

Mentes, A., Szabó, A., Somogyi, B., Vajna, B., Tugyi, N., Csitári, B., Vörös, L., Felföldi, T., 2018. Differences in planktonic microbial communities associated with three types of macrophyte stands in a shallow lake. FEMS Microbiology Ecology94, fix164.

[31]

Mitsch, W.J., Cronk, J.K., Zhang, L., 2014. Creating a living laboratory on a college campus for wetland research–the olentangy river wetland research park, 1991–2012. Ecological Engineering72, 1–10.

[32]

Montesinos-Navarro, A., Hiraldo, F., Tella, J.L., Blanco, G., 2017. Network structure embracing mutualism–antagonism continuums increases community robustness. Nature Ecology & Evolution1, 1661–1669.

[33]

Nelson, C.E., Kelly, L.W., Haas, A.F., 2023. Microbial interactions with dissolved organic matter are central to coral reef ecosystem function and resilience. Annual Review of Marine Science15, 431–460.

[34]

Pang, S., Zhang, S.H., Lv, X.Y., Han, B., Liu, K.H., Qiu, C.H., Wang, C., Wang, P.F., Toland, H., He, Z.L., 2016. Characterization of bacterial community in biofilm and sediments of wetlands dominated by aquatic macrophytes. Ecological Engineering97, 242–250.

[35]

Peter, H., Sommaruga, R., 2016. Shifts in diversity and function of lake bacterial communities upon glacier retreat. The ISME Journal10, 1545–1554.

[36]

Piano, E., Biagioli, F., Nicolosi, G., Coleine, C., Poli, A., Prigione, V., Zanellati, A., Addesso, R., Varese, G.C., Selbmann, L., Isaia, M., 2023. Tourism affects microbial assemblages in show caves. Science of the Total Environment871, 162106.

[37]

R Development Core Team, 2014. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing

[38]

Raza, T., Qadir, M.F., Khan, K.S., Eash, N.S., Yousuf, M., Chatterjee, S., Manzoor, R., Rehman, S.U., Oetting, J.N., 2023. Unrevealing the potential of microbes in decomposition of organic matter and release of carbon in the ecosystem. Journal of Environmental Management344, 118529.

[39]

Russi, D., Brink, P.T., Farmer, A., Badura, T., Coates, D., Förster, J., Kumar, R., Davidson, N., 2013. The economics of ecosystems and biodiversity for water and wetlands. IEEP, London and Brussels, 78.

[40]

Sagova-Mareckova, M., Boenigk, J., Bouchez, A., Cermakova, K., Chonova, T., Cordier, T., Eisendle, U., Elersek, T., Fazi, S., Fleituch, T., Frühe, L., Gajdosova, M., Graupner, N., Haegerbaeumer, A., Kelly, A.M., Kopecky, J., Leese, F., Nõges, P., Orlic, S., Panksep, K., Pawlowski, J., Petrusek, A., Piggott, J.J., Rusch, J.C., Salis, R., Schenk, J., Simek, K., Stovicek, A., Strand, D.A., Vasquez, M.I., Vrålstad, T., Zlatkovic, S., Zupancic, M., Stoeck, T., 2021. Expanding ecological assessment by integrating microorganisms into routine freshwater biomonitoring. Water Research191, 116767.

[41]

Sanna, S., Eja, P., 2017. Recreational cultural ecosystem services: How do people describe the value?. Ecosystem Services26, 1–9.

[42]

Sims, A., Zhang, Y.Y., Gajaraj, S., Brown, P.B., Hu, Z.Q., 2013. Toward the development of microbial indicators for wetland assessment. Water Research47, 1711–1725.

[43]

Spribille, T., Tuovinen, V., Resl, P., Vanderpool, D., Wolinski, H., Aime, M.C., Schneider, K., Stabentheiner, E., Toome-Heller, M., Thor, G., Mayrhofer, H., Johannesson, H., Mccutcheon, J.P., 2016. Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science353, 488–492.

[44]

Sun, P., Wang, Y., Huang, X., Huang, B.Q., Wang, L., 2022. Water masses and their associated temperature and cross-domain biotic factors co-shape upwelling microbial communities. Water Research215, 118274.

[45]

Thackeray, S.J., Hampton, S.E., 2020. The case for research integration, from genomics to remote sensing, to understand biodiversity change and functional dynamics in the world's lakes. Global Change Biology26, 3230–3240.

[46]

Tromas, N., Fortin, N., Bedrani, L., Terrat, Y., Cardoso, P., Bird, D., Greer, C.W., Shapiro, B.J., 2017. Characterising and predicting cyanobacterial blooms in an 8-year amplicon sequencing time course. The ISME Journal11, 1746–1763.

[47]

Wagg, C., Schlaeppi, K., Banerjee, S., Kuramae, E.E., van der Heijden, M.G.A., 2019. Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nature Communications10, 4841.

[48]

Wahlroos, O., Valkama, P., Mäkinen, E., Ojala, A., Vasander, H., Väänänen, V.M., Halonen, A., Lindén, L., Nummi, P., Ahponen, H., Lahti, K., Vessman, T., Rantakokko, K., Nikinmaa, E., 2015. Urban wetland parks in Finland: improving water quality and creating endangered habitats. International Journal of Biodiversity Science, Ecosystem Services & Management11, 46–60.

[49]

Wan, Y., Ruan, X.H., Zhang, Y.P., Li, R.F., 2017. Illumina sequencing-based analysis of sediment bacteria community in different trophic status freshwater lakes. MicrobiologyOpen6, e00450.

[50]

Wang, B.H., Ma, B., Stirling, E., He, Z.L., Zhang, H.J., Yan, Q.Y., 2023a. Freshwater trophic status mediates microbial community assembly and interdomain network complexity. Environmental Pollution316, 120690.

[51]

Wang, B.H., Stirling, E., He, Z.L., Ma, B., Zhang, H.J., Zheng, X.F., Xiao, F.S., Yan, Q.Y., 2021a. Pollution alters methanogenic and methanotrophic communities and increases dissolved methane in small ponds. Science of the Total Environment801, 149723.

[52]

Wang, B.H., Zheng, X.F., Zhang, H.J., Xiao, F.S., Gu, H., Zhang, K.K., He, Z.L., Liu, X., Yan, Q.Y., 2020a. Bacterial community responses to tourism development in the Xixi National Wetland Park, China. Science of the Total Environment720, 137570.

[53]

Wang, B.H., Zheng, X.F., Zhang, H.J., Xiao, F.S., He, Z.L., Yan, Q.Y., 2020b. Keystone taxa of water microbiome respond to environmental quality and predict water contamination. Environmental Research187, 109666.

[54]

Wang, B.H., Zheng, X.F., Zhang, H.J., Yu, X.L., Lian, Y.L., Yang, X.Q., Yu, H., Hu, R.W., He, Z.L., Xiao, F.S., Yan, Q.Y., 2021b. Metagenomic insights into the effects of submerged plants on functional potential of microbial communities in wetland sediments. Marine Life Science & Technology3, 405–415.

[55]

Wang, C., Liu, S.Y., Zhang, Y., Liu, B.Y., He, F., Xu, D., Zhou, Q.H., Wu, Z.B., 2018. Bacterial communities and their predicted functions explain the sediment nitrogen changes along with submerged macrophyte restoration. Microbial Ecology76, 625–636.

[56]

Wang, C., Liu, S.Y., Zhang, Y., Liu, B.Y., Zeng, L., He, F., Zhou, Q.H., Wu, Z.B., 2017. Effects of planted versus naturally growing Vallisneria natans on the sediment microbial community in west lake, China. Microbial Ecology74, 278–288.

[57]

Wang, T., Zhumabieke, M., Zhang, N., Liu, C., Zhong, J.C., Liao, Q.J.H., Zhang, L., 2023b. Variable promotion of algae and macrophyte organic matter on methanogenesis in anaerobic lake sediment. Environmental Research237, 116922.

[58]

Wu, H.P., Hao, B.B., Cai, Y.P., Liu, G.H., Xing, W., 2021. Effects of submerged vegetation on sediment nitrogen-cycling bacterial communities in Honghu Lake (China). Science of the Total Environment755, 142541.

[59]

Wu, H.P., Zeng, G.M., Liang, J., Chen, J., Xu, J.J., Dai, J., Li, X.D., Chen, M., Xu, P., Zhou, Y.Y., Li, F., Hu, L., Wan, J., 2016. Responses of bacterial community and functional marker genes of nitrogen cycling to biochar, compost and combined amendments in soil. Applied Microbiology and Biotechnology100, 8583–8591.

[60]

Wu, H.P., Zeng, G.M., Liang, J., Guo, S.L., Dai, J., Lu, L.H., Wei, Z., Xu, P., Li, F., Yuan, Y.J., He, X.X., 2015. Effect of early dry season induced by the Three Gorges Dam on the soil microbial biomass and bacterial community structure in the Dongting Lake wetland. Ecological Indicators53, 129–136.

[61]

Xue, P.P., Minasny, B., McBratney, A.B., 2022. Land-use affects soil microbial co-occurrence networks and their putative functions. Applied Soil Ecology169, 104184.

[62]

Yu, X.F., E, M.J., Sun, M.Y., Xue, Z.S., Lu, X.G., Jiang, M., Zou, Y.C., 2018. Wetland recreational agriculture: Balancing wetland conservation and agro-development. Environmental Science & Policy87, 11–17.

[63]

Yuan, M.M., Guo, X., Wu, L.W., Zhang, Y., Xiao, N.J., Ning, D.L., Shi, Z., Zhou, X.S., Wu, L.Y., Yang, Y.F., Tiedje, J.M., Zhou, J.Z., 2021a. Climate warming enhances microbial network complexity and stability. Nature Climate Change11, 343–348.

[64]

Yuan, M.M., Kakouridis, A., Starr, E., Nguyen, N., Shi, S.J., Pett-Ridge, J., Nuccio, E., Zhou, J.Z., Firestone, M., 2021b. Fungal-bacterial cooccurrence patterns differ between arbuscular mycorrhizal fungi and nonmycorrhizal fungi across soil niches. mBio12, e03509–20.

[65]

Yun, J.L., Deng, Y.C., Zhang, H.X., 2017. Anthropogenic protection alters the microbiome in intertidal mangrove wetlands in Hainan Island. Applied Microbiology and Biotechnology101, 6241–6252.

[66]

Zeng, L.P., Dai, Y., Zhang, X.M., Man, Y., Tai, Y.P., Yang, Y., Tao, R., 2021. Keystone species and niche differentiation promote microbial N, P, and COD removal in pilot scale constructed wetlands treating domestic sewage. Environmental Science & Technology55, 12652–12663.

[67]

Zhan, P.F., Liu, Y.S., Wang, H.C., Wang, C.L., Xia, M., Wang, N., Cui, W.Z., Xiao, D.R., Wang, H., 2021. Plant litter decomposition in wetlands is closely associated with phyllospheric fungi as revealed by microbial community dynamics and co-occurrence network. Science of the Total Environment753, 142194.

[68]

Zhang, C., Nie, S., Liang, J., Zeng, G.M., Wu, H.P., Hua, S.S., Liu, J.Y., Yuan, Y.J., Xiao, H.B., Deng, L.J., Xiang, H.Y., 2016. Effects of heavy metals and soil physicochemical properties on wetland soil microbial biomass and bacterial community structure. Science of the Total Environment 557–558, 557–558

[69]

Zhang, Z.Q., Yu, H.W., Tao, M., Lv, T., Li, D.X., Yu, D., Liu, C.H., 2023. Shifting enzyme activity and microbial composition in sediment coregulate the structure of an aquatic plant community under polyethylene microplastic exposure. Science of the Total Environment901, 166497.

[70]

Zhao, J.S., Yang, P., Lin, Y.Y., Zhu, X.Y., Wang, J.X., Gan, X.Y., Zheng, X.Y., Zhao, M., Fan, C.Z., Du, L.N., Miu, H.Y., 2023. The effect of underwater supplemental light on the growth of V.spinulosa Yan and the restoration process of water. Process Safety and Environmental Protection169, 328–336.

[71]

Zhou, L., Zhou, Y.Q., Tang, X.M., Zhang, Y.L., Zhu, G.W., Székely, A.J., Jeppesen, E., 2021a. Eutrophication alters bacterial co-occurrence networks and increases the importance of chromophoric dissolved organic matter composition. Limnology and Oceanography66, 2319–2332.

[72]

Zhou, Y.Q., Sun, B.Y., Xie, B.H., Feng, K., Zhang, Z.J., Zhang, Z., Li, S.Z., Du, X.F., Zhang, Q., Gu, S.S., Song, W., Wang, L.L., Xia, J.Y., Han, G.X., Deng, Y., 2021b. Warming reshaped the microbial hierarchical interactions. Global Change Biology27, 6331–6347.

[73]

Zhu, J.L., Li, Y.H., Huang, M.H., Xu, D., Zhang, Y., Zhou, Q.H., Wu, Z.B., Wang, C., 2023. Restoration effects of submerged macrophytes on methane production and oxidation potential of lake sediments. Science of the Total Environment866, 161218.

RIGHTS & PERMISSIONS

Higher Education Press

AI Summary AI Mindmap
PDF (2717KB)

Supplementary files

SEL-00249-OF-HJZ_suppl_1

451

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/