Abiotic and Biotic Drivers of Soil Fungal Communities in Response to Dairy Manure Amendment

Manure amendments in agricultural systems can impact soil microbial communities via supplying growth substrates for indigenous microbes or by introducing manure-borne taxa. This study explores the consistency of these impacts on soil fungal communities and the relative importance of abiotic and biotic drivers across distinct soils. ABSTRACT Modern agriculture often relies on large inputs of synthetic fertilizers to maximize crop yield potential, yet their intensive use has led to nutrient losses and impaired soil health. Alternatively, manure amendments provide plant available nutrients, build organic carbon, and enhance soil health. However, we lack a clear understanding of how consistently manure impacts fungal communities, the mechanisms via which manure impacts soil fungi, and the fate of manure-borne fungi in soils. We assembled soil microcosms using five soils to investigate how manure amendments impact fungal communities over a 60-day incubation. Further, we used autoclaving treatments of soils and manure to determine if observed changes in soil fungal communities were due to abiotic or biotic properties, and if indigenous soil communities constrained colonization of manure-borne fungi. We found that manure amended soil fungal communities diverged from nonamended communities over time, often in concert with a reduction in diversity. Fungal communities responded to live and autoclaved manure in a similar manner, suggesting that abiotic forces are primarily responsible for the observed dynamics. Finally, manure-borne fungi declined quickly in both live and autoclaved soil, indicating that the soil environment is unsuitable for their survival. IMPORTANCE Manure amendments in agricultural systems can impact soil microbial communities via supplying growth substrates for indigenous microbes or by introducing manure-borne taxa. This study explores the consistency of these impacts on soil fungal communities and the relative importance of abiotic and biotic drivers across distinct soils. Different fungal taxa responded to manure among distinct soils, and shifts in soil fungal communities were driven largely by abiotic factors, rather than introduced microbes. This work demonstrates that manure may have inconsistent impacts on indigenous soil fungi, and that abiotic properties of soils render them largely resistant to invasion by manure-borne fungi.

[1]  M. V. D. van der Heijden,et al.  Soil microbiomes and one health , 2022, Nature reviews. Microbiology.

[2]  Xiuping Jiang,et al.  Compositional and Functional Changes in Microbial Communities of Composts Due to the Composting-Related Factors and the Presence of Listeria monocytogenes , 2022, Microbiology spectrum.

[3]  Lei Wu,et al.  Long-term manure application increased soil organic carbon and nitrogen mineralization through the accumulation of unprotected and physically protected carbon fractions , 2022, Pedosphere.

[4]  Xiaomeng Wei,et al.  Application of Manure Rather Than Plant-Origin Organic Fertilizers Alters the Fungal Community in Continuous Cropping Tobacco Soil , 2022, Frontiers in Microbiology.

[5]  G. Krasnov,et al.  Mineral and Organic Fertilizers Distinctly Affect Fungal Communities in the Crop Rhizosphere , 2022, Journal of fungi.

[6]  J. Strengbom,et al.  Links between boreal forest management, soil fungal communities and belowground carbon sequestration , 2021, Functional Ecology.

[7]  K. DeAngelis,et al.  Direct evidence for the role of microbial community composition in the formation of soil organic matter composition and persistence , 2021, ISME Communications.

[8]  G. Krasnov,et al.  Does fresh farmyard manure introduce surviving microbes into soil or activate soil-borne microbiota? , 2021, Journal of environmental management.

[9]  Z. Ye,et al.  Manure Microbial Communities and Resistance Profiles Reconfigure after Transition to Manure Pits and Differ from Those in Fertilized Field Soil , 2021, mBio.

[10]  Q. Shen,et al.  Livestock Manure Type Affects Microbial Community Composition and Assembly During Composting , 2021, Frontiers in Microbiology.

[11]  Q. Zebeli,et al.  The Present Role and New Potentials of Anaerobic Fungi in Ruminant Nutrition , 2021, Journal of fungi.

[12]  Ji‐Zheng He,et al.  Manure application increases microbiome complexity in soil aggregate fractions: Results of an 18-year field experiment , 2021 .

[13]  B. Christensen,et al.  Inconsistent effects of agricultural practices on soil fungal communities across 12 European long‐term experiments , 2021, European Journal of Soil Science.

[14]  Wenxu Dong,et al.  Different contribution of species sorting and exogenous species immigration from manure to soil fungal diversity and community assemblage under long-term fertilization , 2020, Soil Biology and Biochemistry.

[15]  Martti Vasar,et al.  FungalTraits: a user-friendly traits database of fungi and fungus-like stramenopiles , 2020, Fungal Diversity.

[16]  L. Aula,et al.  Livestock Manure and the Impacts on Soil Health: A Review , 2020 .

[17]  N. Fierer,et al.  How microbes can, and cannot, be used to assess soil health , 2020, Soil Biology and Biochemistry.

[18]  E. Otsing,et al.  Regional-Scale In-Depth Analysis of Soil Fungal Diversity Reveals Strong pH and Plant Species Effects in Northern Europe , 2020, Frontiers in Microbiology.

[19]  D. Ahrén,et al.  Uncovering the hidden diversity of litter-decomposition mechanisms in mushroom-forming fungi , 2020, The ISME Journal.

[20]  Zhigao Zhou,et al.  Fungal community structure in relation to manure rate in red soil in southern China , 2020 .

[21]  L. H. Hagen,et al.  Proteome specialization of anaerobic fungi during ruminal degradation of recalcitrant plant fiber , 2020, The ISME Journal.

[22]  Carsten Peterson,et al.  Regulation of fungal decomposition at single-cell level , 2020, The ISME Journal.

[23]  J. Finn,et al.  Biotic resistance to invasion is ubiquitous across ecosystems of the United States. , 2019, Ecology letters.

[24]  A. Howe,et al.  A meta-analysis of global fungal distribution reveals climate-driven patterns , 2019, Nature Communications.

[25]  S. Frey Mycorrhizal Fungi as Mediators of Soil Organic Matter Dynamics , 2019, Annual Review of Ecology, Evolution, and Systematics.

[26]  Muhammad Saleem,et al.  More Than the Sum of Its Parts: Microbiome Biodiversity as a Driver of Plant Growth and Soil Health , 2019, Annual Review of Ecology, Evolution, and Systematics.

[27]  Scott T. Bates,et al.  Fungal functional ecology: bringing a trait‐based approach to plant‐associated fungi , 2019, Biological reviews of the Cambridge Philosophical Society.

[28]  D. Hibbett,et al.  Contemporaneous radiations of fungi and plants linked to symbiosis , 2018, Nature Communications.

[29]  P. Crous,et al.  Redefining Humicola sensu stricto and related genera in the Chaetomiaceae , 2018, Studies in mycology.

[30]  C. Rotz,et al.  Short communication: Identifying challenges and opportunities for improved nutrient management through the USDA's Dairy Agroecosystem Working Group. , 2018, Journal of dairy science.

[31]  M. Jędryczka,et al.  Fungal Biodiversity and Their Role in Soil Health , 2018, Front. Microbiol..

[32]  T. Bruns,et al.  Environmental filtering by pH and soil nutrients drives community assembly in fungi at fine spatial scales , 2017, Molecular ecology.

[33]  Zhong-Liang Wang,et al.  Soil aggregation regulates distributions of carbon, microbial community and enzyme activities after 23-year manure amendment , 2017 .

[34]  J. Gilbert,et al.  Fungal community composition in soils subjected to long-term chemical fertilization is most influenced by the type of organic matter. , 2016, Environmental microbiology.

[35]  Robert C. Edgar,et al.  UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing , 2016, bioRxiv.

[36]  A. Shade Diversity is the question, not the answer , 2016, The ISME Journal.

[37]  Duarte S. Viana,et al.  Disentangling the roles of diversity resistance and priority effects in community assembly , 2016, Oecologia.

[38]  Dan Knights,et al.  Systematic improvement of amplicon marker gene methods for increased accuracy in microbiome studies , 2016, Nature Biotechnology.

[39]  Daryl M. Gohl,et al.  An optimized protocol for high-throughput amplicon-based microbiome profiling , 2016 .

[40]  Bingqiang Zhao,et al.  Temperature effects on soil organic carbon, soil labile organic carbon fractions, and soil enzyme activities under long-term fertilization regimes , 2016 .

[41]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[42]  S. Wuest,et al.  Soil amendments yield persisting effects on the microbial communities—a 7-year study , 2016 .

[43]  Scott T. Bates,et al.  FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild , 2016 .

[44]  S. Sarrocco Dung-inhabiting fungi: a potential reservoir of novel secondary metabolites for the control of plant pathogens. , 2016, Pest management science.

[45]  J. Salles,et al.  Microbial invasions: the process, patterns, and mechanisms. , 2015, Trends in microbiology.

[46]  E. Borer,et al.  Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe , 2015, Proceedings of the National Academy of Sciences.

[47]  K. Treseder,et al.  Fungal Traits That Drive Ecosystem Dynamics on Land , 2015, Microbiology and Molecular Reviews.

[48]  K. Treseder,et al.  Environmental filtering affects soil fungal community composition more than dispersal limitation at regional scales , 2014 .

[49]  R. Henrik Nilsson,et al.  Global diversity and geography of soil fungi , 2014, Science.

[50]  J. Edwards,et al.  Anaerobic fungi (phylum Neocallimastigomycota): advances in understanding their taxonomy, life cycle, ecology, role and biotechnological potential. , 2014, FEMS microbiology ecology.

[51]  R. Evershed,et al.  Crop manuring and intensive land management by Europe’s first farmers , 2013, Proceedings of the National Academy of Sciences.

[52]  X. Zhuang,et al.  Ascomycota Members Dominate Fungal Communities during Straw Residue Decomposition in Arable Soil , 2013, PloS one.

[53]  B. Griffiths,et al.  Insights into the resistance and resilience of the soil microbial community. , 2013, FEMS microbiology reviews.

[54]  P. Baldrian,et al.  Fungal community on decomposing leaf litter undergoes rapid successional changes , 2012, The ISME Journal.

[55]  Matthew G. Bakker,et al.  Harnessing the rhizosphere microbiome through plant breeding and agricultural management , 2012, Plant and Soil.

[56]  Q. Shen,et al.  Control of cotton Verticillium wilt and fungal diversity of rhizosphere soils by bio-organic fertilizer , 2012, Biology and Fertility of Soils.

[57]  A. Good,et al.  Fertilizing Nature: A Tragedy of Excess in the Commons , 2011, PLoS biology.

[58]  G. Bonanomi,et al.  Identifying the characteristics of organic soil amendments that suppress soilborne plant diseases. , 2010 .

[59]  F. Magdoff,et al.  Autoclaving soil samples affects algal-available phosphorus. , 2005, Journal of environmental quality.

[60]  S. Rosendahl,et al.  Population structure and pathogenicity of members of the Fusarium oxysporum complex isolated from soil and root necrosis of pea (Pisum sativum L.). , 2002, FEMS microbiology ecology.

[61]  D. Davies,et al.  The survival of anaerobic fungi in cattle faeces , 1999 .

[62]  D. Wynn-Williams,et al.  Ecological and physiological characterization of Humicola marvinii, a new psychrophilic fungus from fellfield soils in the maritime Antarctic , 1997 .

[63]  R. Vilgalys,et al.  Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species , 1990, Journal of bacteriology.

[64]  Melissa L. Wilson,et al.  Abiotic and biotic filters determine the response of soil bacterial communities to manure amendment , 2022, Applied Soil Ecology.

[65]  J. B. Robinson,et al.  A comparison of autoclaved and gamma-irradiated soils as media for microbial colonization experiments , 2005, Plant and Soil.

[66]  Robert C. Edgar,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2001 .

[67]  J. Tisdall,et al.  Aggregation of soil by fungal hyphae , 1997 .

[68]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[69]  T. White Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics , 1990 .

[70]  Rothamsted Repository Download , 2022 .