in

Stronger responses of soil protistan communities to legacy mercury pollution than bacterial and fungal communities in agricultural systems

  • van Elsas JD, Chiurazzi M, Mallon CA, Elhottovā D, Krištůfek V, Salles JF. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc Natl Acad Sci USA 2012;109:1159–64.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Bardgett RD, Van Der Putten WH. Belowground biodiversity and ecosystem functioning. Nature. 2014;515:505–11.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • George PB, Lallias D, Creer S, Seaton FM, Kenny JG, Eccles RM, et al. Divergent national-scale trends of microbial and animal biodiversity revealed across diverse temperate soil ecosystems. Nat Commun. 2019;10:1–11.

    Article 
    CAS 

    Google Scholar 

  • Delgado-Baquerizo M, Reich PB, Trivedi C, Eldridge DJ, Abades S, Alfaro FD, et al. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nat Ecol Evol. 2020;4:210–20.

    PubMed 
    Article 

    Google Scholar 

  • Xiao E, Ning Z, Xiao T, Sun W, Jiang S. Soil bacterial community functions and distribution after mining disturbance. Soil Biol Biochem. 2021;157:108232.

    CAS 
    Article 

    Google Scholar 

  • Jiao S, Zhang Z, Yang F, Lin Y, Chen W, Wei G. Temporal dynamics of microbial communities in microcosms in response to pollutants. Mol Ecol. 2017;26:923–36.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Fajardo C, Costa G, Nande M, Botías P, García-Cantalejo J, Martín M. Pb, Cd, and Zn soil contamination: monitoring functional and structural impacts on the microbiome. Appl Soil Ecol. 2019;135:56–64.

    Article 

    Google Scholar 

  • Krabbenhoft DP, Sunderland EM. Global change and mercury. Science. 2013;341:1457–8.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Obrist D, Kirk JL, Zhang L, Sunderland EM, Jiskra M, Selin NE. A review of global environmental mercury processes in response to human and natural perturbations: Changes of emissions, climate, and land use. Ambio. 2018;47:116–40.

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Amos HM, Jacob DJ, Streets DG, Sunderland EM. Legacy impacts of all-time anthropogenic emissions on the global mercury cycle. Global Biogeochem Cycles. 2013;27:410–21.

    CAS 
    Article 

    Google Scholar 

  • Zhang L, Wong MH. Environmental mercury contamination in China: sources and impacts. Environ Int. 2007;33:108–21.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Müller AK, Westergaard K, Christensen S, Sørensen SJ. The effect of long-term mercury pollution on the soil microbial community. FEMS Microbiol Ecol. 2001;36:11–9.

    PubMed 
    Article 

    Google Scholar 

  • Liu YR, Wang JJ, Zheng YM, Zhang LM, He JZ. Patterns of bacterial diversity along a long-term mercury-contaminated gradient in the paddy soils. Microb Ecol. 2014;68:575–83.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Liu YR, Delgado-Baquerizo M, Bi L, Zhu J, He JZ. Consistent responses of soil microbial taxonomic and functional attributes to mercury pollution across China. Microbiome. 2018;6:183.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Li D, Li X, Tao Y, Yan Z, Ao Y. Deciphering the bacterial microbiome in response to long-term mercury contaminated soil. Ecotoxicol Environ Saf. 2022;229:113062.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Zappelini C, Karimi B, Foulon J, Lacercat-Didier L, Maillard F, Valot B, et al. Diversity and complexity of microbial communities from a chlor-alkali tailings dump. Soil Biol Biochem. 2015;90:101–10.

    CAS 
    Article 

    Google Scholar 

  • Baldrian P, in der Wiesche C, Gabriel J, Nerud F, Zadražil F. Influence of cadmium and mercury on activities of ligninolytic enzymes and degradation of polycyclic aromatic hydrocarbons by Pleurotus ostreatus in soil. Appl Environ Microbiol. 2000;66:2471–8.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Crane S, Dighton J, Barkay T. Growth responses to and accumulation of mercury by ectomycorrhizal fungi. Fungal Biol. 2010;114:873–80.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Johansen JL, Rønn R, Ekelund F. Toxicity of cadmium and zinc to small soil protists. Environ Pollut. 2018;242:1510–7.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Wanner M, Birkhofer K, Fischer T, Shimizu M, Shimano S, Puppe D. Soil testate amoebae and diatoms as bioindicators of an old heavy metal contaminated floodplain in Japan. Microb Ecol. 2020;79:123–33.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Zhou Y, Sun B, Xie B, Feng K, Zhang Z, Zhang Z, et al. Warming reshaped the microbial hierarchical interactions. Glob Chang Biol. 2021;27:6331–47.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Zhao ZB, He JZ, Geisen S, Han LL, Wang JT, Shen JP, et al. Protist communities are more sensitive to nitrogen fertilization than other microorganisms in diverse agricultural soils. Microbiome. 2019;7:33.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Geisen S, Mitchell EAD, Adl S, Bonkowski M, Dunthorn M, Ekelund F, et al. Soil protists: a fertile frontier in soil biology research. FEMS Microbiol Rev. 2018;42:293–323.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Jiang Y, Luan L, Hu K, Liu M, Chen Z, Geisen S, et al. Trophic interactions as determinants of the arbuscular mycorrhizal fungal community with cascading plant-promoting consequences. Microbiome. 2020;8:1–14.

    CAS 
    Article 

    Google Scholar 

  • Huang X, Wang J, Dumack K, Liu W, Zhang Q, He Y, et al. Protists modulate fungal community assembly in paddy soils across climatic zones at the continental scale. Soil Biol Biochem. 2021;160:108358.

    CAS 
    Article 

    Google Scholar 

  • Grossmann L, Jensen M, Heider D, Jost S, Glücksman E, Hartikainen H, et al. Protistan community analysis: key findings of a large-scale molecular sampling. ISME J. 2016;10:2269–79.

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Jassey VE, Signarbieux C, Hättenschwiler S, Bragazza L, Buttler A, Delarue F, et al. An unexpected role for mixotrophs in the response of peatland carbon cycling to climate warming. Sci Rep. 2015;5:1–10.

    Article 
    CAS 

    Google Scholar 

  • Thakur MP, Geisen S. Trophic regulations of the soil microbiome. Trends Microbiol. 2019;27:771–80.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Geisen S, Hu S, Dela Cruz TEE, Veen GFC. Protists as catalyzers of microbial litter breakdown and carbon cycling at different temperature regimes. ISME J. 2021;15:618–21.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Guo S, Xiong W, Hang X, Gao Z, Jiao Z, Liu H, et al. Protists as main indicators and determinants of plant performance. Microbiome. 2021;9:64.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Feng X, Li P, Qiu G, Wang S, Li G, Shang L, et al. Human exposure to methylmercury through rice intake in mercury mining areas, Guizhou Province, China. Environ Sci Technol. 2008;42:326–32.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Meng M, Li B, Shao JJ, Wang T, He B, Shi JB, et al. Accumulation of total mercury and methylmercury in rice plants collected from different mining areas in China. Environ Pollut. 2014;184:179–86.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Liu YR, Dong JX, Zhang QG, Wang JT, Han LL, Zeng J, et al. Longitudinal occurrence of methylmercury in terrestrial ecosystems of the Tibetan Plateau. Environ Pollut. 2016;218:1342–9.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Walkley A, Black IA. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci. 1934;37:29–38.

    CAS 
    Article 

    Google Scholar 

  • Jones D, Willett V. Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem. 2006;38:991–9.

    CAS 
    Article 

    Google Scholar 

  • Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, et al. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun. 2016;7:1–8.

    Article 
    CAS 

    Google Scholar 

  • Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol. 1993;2:113–8.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Stoeck T, Bass D, Nebel M, Christen R, Jones MD, Breiner H-W, et al. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol. 2010;19:21–31.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–D6.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Nilsson RH, Larsson K-H, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, et al. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res. 2019;47:D259–D64.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, et al. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 2013;41:D597–604.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Oliverio AM, Geisen S, Delgado-Baquerizo M, Maestre FT, Turner BL, Fierer N. The global-scale distributions of soil protists and their contributions to belowground systems. Sci Adv. 2020;6:eaax8787.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Finland MotE: Government decree on the assessment of soil contamination and remediation needs (214/2007). In.: Ministry of the Environment Helsinki (FI); 2007.

  • Carlon C. Derivation methods of soil screening values in europe: A review of national procedures towards harmonisation: A report of the ENSURE action. EUR-OP. 2007.

  • Toth G, Hermann T, Da Silva MR, Montanarella L. Heavy metals in agricultural soils of the European Union with implications for food safety. Environ Int. 2016;88:299–309.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • De Caceres M, Jansen F. Relationship between species and groups of sites. Package ‘indicspecies’, version 1.7.6. 2016.

  • Frossard A, Donhauser J, Mestrot A, Gygax S, Bååth E, Frey B. Long-and short-term effects of mercury pollution on the soil microbiome. Soil Biol Biochem. 2018;120:191–9.

    CAS 
    Article 

    Google Scholar 

  • Ma B, Wang H, Dsouza M, Lou J, He Y, Dai Z, et al. Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China. ISME J. 2016;10:1891–901.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Langfelder P, Horvath S. Fast R functions for robust correlations and hierarchical clustering. J Stat Softw. 2012;46:1–17.

    Article 

    Google Scholar 

  • Luo F, Zhong J, Yang Y, Scheuermann RH, Zhou J. Application of random matrix theory to biological networks. Phys Lett A. 2006;357:420–3.

    CAS 
    Article 

    Google Scholar 

  • Deng Y, Jiang YH, Yang YF, He ZL, Luo F, Zhou JZ. Molecular ecological network analyses. BMC Bioinform. 2012;13:1–20.

    Article 

    Google Scholar 

  • Benjamini Y, Krieger AM, Yekutieli D. Adaptive linear step-up procedures that control the false discovery rate. Biometrika. 2006;93:491–507.

    Article 

    Google Scholar 

  • Bastian M, Heymann S, Jacomy M. Gephi: an open source software for exploring and manipulating networks. Proceedings of the International AAAI Conference on Web and Social Media. 2009;3:361–2.

  • Csardi G, Nepusz T. The igraph software package for complex network research. InterJ Complex Syst. 2006;1695:1–9.

    Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin P, O’Hara R, et al. Vegan: community ecology package. Ordination methods, diversity analysis and other functions for community and vegetation ecologists. R Package Ver. 2015;2:3–1.

    Google Scholar 

  • Chen B, Xiong W, Qi J, Pan H, Chen S, Peng Z, et al. Trophic interrelationships drive the biogeography of protistan community in agricultural ecosystems. Soil Biol Biochem. 2021;163:108445.

    CAS 
    Article 

    Google Scholar 

  • Jiao S, Lu Y, Wei G. Soil multitrophic network complexity enhances the link between biodiversity and multifunctionality in agricultural systems. Glob Chang Biol. 2022;28:140–53.

  • Sunagawa S, Coelho LP, Chaffron S, Kultima JR, Labadie K, Salazar G, et al. Structure and function of the global ocean microbiome. Science. 2015;348:1261359.

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Revelle WR. psych: Procedures for personality and psychological research. 2017.

  • Archer E. rfPermute: estimate permutation p-values for random forest importance metrics. R package version. 2016;1(2).

  • Wang JT, Zheng YM, Hu HW, Li J, Zhang LM, Chen BD, et al. Coupling of soil prokaryotic diversity and plant diversity across latitudinal forest ecosystems. Sci Rep. 2016;6:1–7.

    Article 
    CAS 

    Google Scholar 

  • Schermelleh-Engel K, Moosbrugger H, Müller H. Evaluating the fit of structural equation models: Tests of significance and descriptive goodness-of-fit measures. Methods Psychol Res Online. 2003;8:23–74.

    Google Scholar 

  • Zinger L, Taberlet P, Schimann H, Bonin A, Boyer F, De Barba M, et al. Body size determines soil community assembly in a tropical forest. Mol Ecol. 2019;28:528–43.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Stefan G, Cornelia B, Jörg R, Michael B. Soil water availability strongly alters the community composition of soil protists. Pedobiologia. 2014;57:205–13.

    Article 

    Google Scholar 

  • Luan L, Jiang Y, Cheng M, Dini-Andreote F, Sui Y, Xu Q, et al. Organism body size structures the soil microbial and nematode community assembly at a continental and global scale. Nat Commun. 2020;11:6406.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Qi Q, Hu C, Lin J, Wang X, Tang C, Dai Z, et al. Contamination with multiple heavy metals decreases microbial diversity and favors generalists as the keystones in microbial occurrence networks. Environ Pollut. 2022;306:119406.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Wu W, Lu HP, Sastri A, Yeh YC, Gong GC, Chou WC, et al. Contrasting the relative importance of species sorting and dispersal limitation in shaping marine bacterial versus protist communities. ISME J. 2018;12:485–94.

    PubMed 
    Article 

    Google Scholar 

  • Villarino E, Watson JR, Jönsson B, Gasol JM, Salazar G, Acinas SG, et al. Large-scale ocean connectivity and planktonic body size. Nat Commun. 2018;9:1–13.

    CAS 
    Article 

    Google Scholar 

  • Mitsch WJ, Gosselink JG Wetlands. John Wiley & Sons; 2015.

  • Margesin R, Feller G, Gerday C, Russell N. The Encyclopedia of Environmental Microbiology. 2002;2.

  • Liu YR, Johs A, Bi L, Lu X, Hu HW, Sun D, et al. Unraveling microbial communities associated with methylmercury production in paddy soils. Environ Sci Technol. 2018;52:13110–8.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Hall B, St Louis V, Rolfhus K, Bodaly R, Beaty K, Paterson M, et al. Impacts of reservoir creation on the biogeochemical cycling of methyl mercury and total mercury in boreal upland forests. Ecosystems. 2005;8:248–66.

    CAS 
    Article 

    Google Scholar 

  • Clarholm M. Protozoan grazing of bacteria in soil-impact and importance. Microb Ecol. 1981;7:343–50.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Asiloglu R, Shiroishi K, Suzuki K, Turgay OC, Harada N. Soil properties have more significant effects on the community composition of protists than the rhizosphere effect of rice plants in alkaline paddy field soils. Soil Biol Biochem. 2021;161:108397.

    CAS 
    Article 

    Google Scholar 

  • Asiloglu R, Kenya K, Samuel SO, Sevilir B, Murase J, Suzuki K, et al. Top-down effects of protists are greater than bottom-up effects of fertilisers on the formation of bacterial communities in a paddy field soil. Soil Biol Biochem. 2021;156:108186.

    CAS 
    Article 

    Google Scholar 

  • Nguyen BAT, Chen QL, He JZ, Hu HW. Livestock manure spiked with the antibiotic tylosin significantly altered soil protist functional groups. J Hazard Mater. 2021;427:127867.

  • Nguyen BAT, Chen QL, He JZ, Hu HW. Oxytetracycline and ciprofloxacin exposure altered the composition of protistan consumers in an agricultural soil. Environ Sci Technol. 2020;54:9556–63.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Nguyen BAT, Chen QL, Yan ZZ, Li CY, He JZ, Hu HW. Distinct factors drive the diversity and composition of protistan consumers and phototrophs in natural soil ecosystems. Soil Biol Biochem. 2021;160:108317.

    CAS 
    Article 

    Google Scholar 

  • Wu S, Dong Y, Deng Y, Cui L, Zhuang X. Protistan consumers and phototrophs are more sensitive than bacteria and fungi to pyrene exposure in soil. Sci Total Environ. 2022;822:153539.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Potts LD, Douglas A, Perez Calderon LJ, Anderson JA, Witte U, Prosser JI, et al. Chronic environmental perturbation influences microbial community assembly patterns. Environ Sci Technol. 2022;56:2300–11.

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Ge AH, Liang ZH, Xiao JL, Zhang Y, Zeng Q, Xiong C, et al. Microbial assembly and association network in watermelon rhizosphere after soil fumigation for Fusarium wilt control. Agric Ecosyst Environ. 2021;312:107336.

    CAS 
    Article 

    Google Scholar 

  • Pernthaler J, Sattler B, Simek K, Schwarzenbacher A, Psenner R. Top-down effects on the size-biomass distribution of a freshwater bacterioplankton community. Aquat Microb Ecol. 1996;10:255–63.

    Article 

    Google Scholar 

  • Holtze MS, Ekelund F, Rasmussen LD, Jacobsen CS, Johnsen K. Prey-predator dynamics in communities of culturable soil bacteria and protozoa: differential effects of mercury. Soil Biol Biochem. 2003;35:1175–81.

    CAS 
    Article 

    Google Scholar 

  • Fuhrman JA. Microbial community structure and its functional implications. Nature. 2009;459:193–9.

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Meisner A, Wepner B, Kostic T, van Overbeek LS, Bunthof CJ, de Souza RSC, et al. Calling for a systems approach in microbiome research and innovation. Curr Opin Biotechnol. 2022;73:171–8.

    CAS 
    PubMed 
    Article 

    Google Scholar 


  • Source: Ecology - nature.com

    Distribution model transferability for a wide-ranging species, the Gray Wolf

    New J-WAFS-led project combats food insecurity