Salinization influences the biodiversity-ecosystem functioning relationship more strongly at high salinity

Abstract

Salinization threatens ecosystem stability by altering microbial diversity and function, yet how salinity influences biodiversity-ecosystem functioning (BEF) relationships remains unclear. In this study, we constructed artificial microbial communities (5–40 strains) with varying salt tolerance and phylogeny, culturing them across a salinity gradient (0.9%–20%). We found that low-to-moderate salinity (0.9%–7%) minimally affected BEF relationships, but high salinity (15%–20%) amplified biodiversity loss impacts, with ecosystem yield declining sharply at low richness (R² = 0.573, p < 0.001). Hypersaline conditions shifted community composition toward halophiles (e.g., Halomonas dominance at 20% salinity) and inhibited metabolic functions, such as glycosyl hydrolase activity. Mechanistically, selection effects predominated at 15% salinity (contributing 63.1%–72.0% to net biodiversity effects), whereas complementarity effects were diminished. These findings underscore the vital role of biodiversity in mitigating hypersaline stress and highlight the necessity for targeted strategies to enhance ecosystem resilience against global salinization.

Keywords

community assembly / environmental filtering / functional redundancy / microbial diversity / osmotic stress

References

[1] Ondrasek G, Rengel Z. Environmental salinization processes: detection, implications & solutions. Sci Total Environ. 2021; 754:142432.

[2] Hassani A, Azapagic A, Shokri N. Global predictions of primary soil salinization under changing climate in the 21st century. Nat Commun. 2021; 12: 6663.

[3] Cañedo-Argüelles M. A review of recent advances and future challenges in freshwater salinization. Limnetica. 2020; 39: 185–211.

[4] Vengosh A. 11.9 - Salinization and saline environments. In: HD Holland, KK Turekian, editors. Treatise on geochemistry (Second Edition). Oxford: Elsevier; 2014. p. 325–378.

[5] Perri S, Molini A, Hedin LO, Porporato A. Contrasting effects of aridity and seasonality on global salinization. Nat Geosci. 2022; 15: 375–381.

[6] Huang J, Yang J, Jiang H, Wu G, Liu W, Wang B, et al. Microbial responses to simulated salinization and desalinization in the sediments of the Qinghai-Tibetan Lakes. Front Microbiol. 2020; 11: 1772.

[7] Zhang G, Bai J, Tebbe CC, Zhao Q, Jia J, Wang W, et al. Salinity controls soil microbial community structure and function in coastal estuarine wetlands. Environ Microbiol. 2021; 23: 1020–1037.

[8] Rath KM, Rousk J. Salt effects on the soil microbial decomposer community and their role in organic carbon cycling: a review. Soil Biol Biochem. 2015; 81: 108–123.

[9] Chen H, Ma K, Huang Y, Yang Y, Ma Z, Chu C. Salinity drives functional and taxonomic diversities in global water metagenomes. Front Microbiol. 2021; 12:719725.

[10] Zhang K, Shi Y, Cui X, Yue P, Li K, Liu X, et al. Salinity is a key determinant for soil microbial communities in a desert ecosystem. mSystems. 2019; 4:e00225-00218.

[11] Jiang H, Huang J, Li L, Huang L, Manzoor M, Yang J, et al. Onshore soil microbes and endophytes respond differently to geochemical and mineralogical changes in the Aral Sea. Sci Total Environ. 2021; 765:142675.

[12] Yang Y, Moorhead DL, Craig H, Luo M, Chen X, Huang J, et al. Differential responses of soil extracellular enzyme activities to salinization: implications for soil carbon cycling in tidal wetlands. Global Biogeochem Cycles. 2022; 36:e2021GB007285.

[13] Sun X, Tan E, Wang B, Gan Z, Yang J, Han J, et al. Salinity change induces distinct climate feedbacks of nitrogen removal in saline lakes. Water Res. 2023; 245:120668.

[14] Loreau M. Biodiversity and ecosystem functioning: recent theoretical advances. Oikos. 2000; 91: 3–17.

[15] Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monograph. 2005; 75: 3–35.

[16] Gamfeldt L, Lefcheck JS, Byrnes JEK, Cardinale BJ, Duffy JE, Griffin JN. Marine biodiversity and ecosystem functioning: what's known and what's next? Oikos. 2015; 124: 252–265.

[17] Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, et al. Biodiversity loss and its impact on humanity. Nature. 2012; 486: 59–67.

[18] van der Plas F. Biodiversity and ecosystem functioning in naturally assembled communities. Biological Reviews. 2019; 94: 1220–1245.

[19] Awasthi A, Singh M, Soni SK, Singh R, Kalra A. Biodiversity acts as insurance of productivity of bacterial communities under abiotic perturbations. ISME J. 2014; 8: 2445–2452.

[20] Loreau M, Mouquet N, Gonzalez A. Biodiversity as spatial insurance in heterogeneous landscapes. Proc Natl Acad Sci USA. 2003; 100: 12765–12770.

[21] Steudel B, Hector A, Friedl T, Löfke C, Lorenz M, Wesche M, et al. Biodiversity effects on ecosystem functioning change along environmental stress gradients. Ecol Lett. 2012; 15: 1397–1405.

[22] Loreau M, Hector A. Partitioning selection and complementarity in biodiversity experiments. Nature. 2001; 412: 72–76.

[23] Zhang WP, Gao SN, Li ZX, Xu HS, Yang H, Yang X, et al. Shifts from complementarity to selection effects maintain high productivity in maize/legume intercropping systems. J Appl Ecol. 2021; 58: 2603–2613.

[24] García FC, Bestion E, Warfield R, Yvon-Durocher G. Changes in temperature alter the relationship between biodiversity and ecosystem functioning. Proc Natl Acad Sci USA. 2018; 115: 10989–10994.

[25] Raynaud T, Devers-Lamrani M, Spor A, Blouin M. Community diversity determines the evolution of synthetic bacterial communities under artificial selection. Evolution. 2022; 76: 1883–1895.

[26] Saleem M, Fetzer I, Dormann CF, Harms H, Chatzinotas A. Predator richness increases the effect of prey diversity on prey yield. Nat Commun. 2012; 3: 1305.

[27] Venail PA, Vives MJ. Positive effects of bacterial diversity on ecosystem functioning driven by complementarity effects in a bioremediation context. PLoS One. 2013; 8:e72561.

[28] Jiang L. Negative selection effects suppress relationships between bacterial diversity and ecosystem functioning. Ecology. 2007; 88: 1075–1085.

[29] Evans R, Alessi AM, Bird S, McQueen-Mason SJ, Bruce NC, Brockhurst MA. Defining the functional traits that drive bacterial decomposer community productivity. ISME J. 2017; 11: 1680–1687.

[30] Salles JF, Poly F, Schmid B, Roux XL. Community niche predicts the functioning of denitrifying bacterial assemblages. Ecology. 2009; 90: 3324–3332.

[31] Isbell F, Reich PB, Tilman D, Hobbie SE, Polasky S, Binder S. Nutrient enrichment, biodiversity loss, and consequent declines in ecosystem productivity. Proc Natl Acad Sci USA. 2013; 110: 11911–11916.

[32] Hong P, Schmid B, De Laender F, Eisenhauer N, Zhang X, Chen H, et al. Biodiversity promotes ecosystem functioning despite environmental change. Ecol Lett. 2022; 25: 555–569.

[33] Tilman D. Resource competition and community structure. Princeton: Princeton University Press; 1982.

[34] Ratcliffe S, Wirth C, Jucker T, van der Plas F, Scherer-Lorenzen M, Verheyen K, et al. Biodiversity and ecosystem functioning relations in European forests depend on environmental context. Ecol Lett. 2017; 20: 1414–1426.

[35] Langenheder S, Bulling MT, Solan M, Prosser JI. Bacterial biodiversity ecosystem functioning relations are modified by environmental complexity. PLoS One. 2010; 5:e10834.

[36] Loreau M, de Mazancourt C. Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecol Lett. 2013; 16: 106–115.

[37] Tilman D, Reich PB, Knops JMH. Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature. 2006; 441: 629–632.

[38] Yachi S, Loreau M. Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci USA. 1999; 96: 1463–1468.

[39] Tilman D, Isbell F, Cowles JM. Biodiversity and ecosystem functioning. Ann Rev Ecol Evol Syst. 2014; 45: 471–493.

[40] Batrich M, Maskeri L, Schubert R, Ho B, Kohout M, Abdeljaber M, et al. Pseudomonas diversity within urban freshwaters. Front Microbiol. 2019; 10: 195.

[41] Pietsch RB, Vinatzer BA, Schmale III DG. Diversity and abundance of ice-nucleating strains of Pseudomonas syringae in a freshwater lake in Virginia, USA. Front Microbiol. 2017; 8: 318.

[42] Baik KS, Lim CH, Choe HN, Kim EM, Seong CN. Paenibacillus rigui sp. nov., isolated from a freshwater wetland. Int J Syst Evol Microbiol. 2011; 61: 529–534.

[43] Xu XW, Wu YH, Zhou Z, Wang CS, Zhou YG, Zhang HB, et al. Halomonas saccharevitans sp. nov., Halomonas arcis sp. nov. and Halomonas subterranea sp. nov., halophilic bacteria isolated from hypersaline environments of China. Int J Syst Evol Microbiol. 2007; 57: 1619–1624.

[44] Vishnuvardhan Reddy S, Thirumala M, Farooq M, Sasikala C, Venkata Ramana C. Marinococcus salis sp., nov., a moderately halophilic bacterium isolated from a salt marsh. Arch Microbiol. 2016; 198: 1013–1018.

[45] Wang T, Jiang Z, Dong W, Liang X, Zhang L, Zhu Y. Growth and nitrogen removal characteristics of Halomonas sp. B01 under high salinity. Ann Microbiol. 2019; 69: 1425–1433.

[46] Wang Y, Cao LL, Tang SK, Lou K, Mao PH, Jin X, et al. Marinococcus luteus sp. nov., a halotolerant bacterium isolated from a salt lake, and emended description of the genus Marinococcus. Int J Syst Evol Microbiol. 2009; 59: 2875–2879.

[47] Huang J, Han M, Yang J, Kappler A, Jiang H. Salinity impact on composition and activity of nitrate-reducing Fe(II)-oxidizing microorganisms in saline lakes. Appl Environ Microbiol. 2022; 88:e00132-00122.

[48] Wu QL, Zwart G, Schauer M, Kamst-van Agterveld MP, Hahn MW. Bacterioplankton community composition along a salinity gradient of sixteen high-mountain lakes located on the Tibetan Plateau, China. Appl Environ Microbiol. 2006; 72: 5478–5485.

[49] Cook FJ, Orchard VA. Relationships between soil respiration and soil moisture. Soil Biol Biochem. 2008; 40: 1013–1018.

[50] Baumann K, Marschner P. Effects of salinity on microbial tolerance to drying and rewetting. Biogeochemistry. 2013; 112: 71–80.

[51] Logares R, Tesson SVM, Canbäck B, Pontarp M, Hedlund K, Rengefors K. Contrasting prevalence of selection and drift in the community structuring of bacteria and microbial eukaryotes. Environ Microbiol. 2018; 20: 2231–2240.

[52] Dupont CL, Larsson J, Yooseph S, Ininbergs K, Goll J, Asplund-Samuelsson J, et al. Functional tradeoffs underpin salinity-driven divergence in microbial community composition. PLoS One. 2014; 9:e89549.

[53] Singh K. Microbial and enzyme activities of saline and sodic soils. Land Degr Dev. 2016; 27: 706–718.

[54] Frankenberger Jr. WT, Bingham FT. Influence of salinity on soil enzyme activities. Soil Sci Am J. 1982; 46: 1173–1177.

[55] Liu W, Jiang H, Yang J, Wu G. Gammaproteobacterial diversity and carbon utilization in response to salinity in the Lakes on the Qinghai-Tibetan Plateau. Geomicrobiol J. 2018; 35: 392–403.

[56] Oren A. Thermodynamic limits to microbial life at high salt concentrations. Environ Microbiol. 2011; 13: 1908–1923.

[57] Campo P, Platten W III, Suidan MT, Chai Y, Davis JW. Aerobic biodegradation of amines in industrial saline wastewaters. Chemosphere. 2011; 85: 1199–1203.

[58] Castillo-Carvajal LC, Sanz-Martín JL, Barragán-Huerta BE. Biodegradation of organic pollutants in saline wastewater by halophilic microorganisms: a review. Environ Sci Pollut Res. 2014; 21: 9578–9588.

[59] Wang S, Isbell F, Deng W, Hong P, Dee LE, Thompson P, et al. How complementarity and selection affect the relationship between ecosystem functioning and stability. Ecology. 2021; 102:e03347.

[60] Tilman D, Lehman CL, Thomson KT. Plant diversity and ecosystem productivity: theoretical considerations. Proc Natl Acad Sci USA. 1997; 94: 1857–1861.

[61] Špaèková I, Lepš J. Procedure for separating the selection effect from other effects in diversity–productivity relationship. Ecol Lett. 2001; 4: 585–594.

[62] Fargione J, Tilman D, Dybzinski R, Lambers JHR, Clark C, Harpole WS, et al. From selection to complementarity: shifts in the causes of biodiversity–productivity relationships in a long-term biodiversity experiment. Proc R Soc B. 2007; 274: 871–876.

[63] Li XF, Wang CB, Zhang WP, Wang LH, Tian XL, Yang SC, et al. The role of complementarity and selection effects in P acquisition of intercropping systems. Plant Soil. 2018; 422: 479–493.

[64] Yang J, Jiang H, Liu W, Huang L, Huang J, Wang B, et al. Potential utilization of terrestrially derived dissolved organic matter by aquatic microbial communities in saline lakes. ISME J. 2020; 14: 2313–2324.

[65] Jiang H, Huang J, Yang J. Halotolerant and halophilic microbes and their environmental implications in saline and hypersaline lakes in Qinghai Province, China. In: D Egamberdieva, N Birkeland, H Panosyan, W Li, editors. Extremophiles in Eurasian ecosystems: ecology, diversity, and applications. Singapore: Springer; 2018. p. 299–316.

[66] Jiang H, Dong H, Zhang G, Yu B, Chapman LR, Fields MW. Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China. Appl Environ Microbiol. 2006; 72: 3832–3845.

[67] Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4: 406–425.

[68] Yu G, Smith DK, Zhu H, Guan Y, Lam TTY. ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol. 2017; 8: 28–36.

[69] Isbell F, Cowles J, Dee LE, Loreau M, Reich PB, Gonzalez A, et al. Quantifying effects of biodiversity on ecosystem functioning across times and places. Ecol Lett. 2018; 21: 763–778.

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