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      Site‐specific responses of foliar fungal microbiomes to nutrient addition and herbivory at different spatial scales

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          Abstract

          The plant microbiome can affect host function in many ways and characterizing the ecological factors that shape endophytic (microbes living inside host plant tissues) community diversity is a key step in understanding the impacts of environmental change on these communities. Phylogenetic relatedness among members of a community offers a way of quantifying phylogenetic diversity of a community and can provide insight into the ecological factors that shape endophyte microbiomes. We examined the effects of experimental nutrient addition and herbivory exclusion on the phylogenetic diversity of foliar fungal endophyte communities of the grass species Andropogon gerardii at four sites in the Great Plains of the central USA. Using amplicon sequencing, we characterized the effects of fertilization and herbivory on fungal community phylogenetic diversity at spatial scales that spanned within‐host to between sites across the Great Plains. Despite increasing fungal diversity and richness, at larger spatial scales, fungal microbiomes were composed of taxa showing random phylogenetic associations. Phylogenetic diversity did not differ systematically when summed across increasing spatial scales from a few meters within plots to hundreds of kilometers among sites. We observed substantial shifts in composition across sites, demonstrating distinct but similarly diverse fungal communities were maintained within sites across the region. In contrast, at the scale of within leaves, fungal communities tended to be comprised of closely related taxa regardless of the environment, but there were no shifts in phylogenetic composition among communities. We also found that nutrient addition (fertilization) and herbivory have varying effects at different sites. These results suggest that the direction and magnitude of the outcomes of environmental modifications likely depend on the spatial scale considered, and can also be constrained by regional site differences in microbial diversity and composition.

          Abstract

          The plant microbiome can affect host function in many ways yet our understanding of the ecological and environmental factors that shape plant microbiomes is limited, especially within the evolutionary context of phylogenetic relatedness among members of a community. We characterized the responses of foliar fungal endophytic microbiomes of Andropogon gerardii to nutrient addition and herbivory at different spatial scales in a distributed, regional‐scale experiment. Despite increasing fungal diversity and richness, phylogenetic diversity of fungal microbiomes did not differ systematically when summed across increasing spatial scales although nutrient addition and herbivory have varying effects at different sites, suggesting that that the direction and magnitude of the outcomes of environmental modifications likely depend on the spatial scale considered and can also be constrained by regional site differences in microbial diversity and composition.

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          Most cited references35

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          Opposing effects of competitive exclusion on the phylogenetic structure of communities.

          Though many processes are involved in determining which species coexist and assemble into communities, competition is among the best studied. One hypothesis about competition's contribution to community assembly is that more closely related species are less likely to coexist. Though empirical evidence for this hypothesis is mixed, it remains a common assumption in certain phylogenetic approaches for inferring the effects of environmental filtering and competitive exclusion. Here, we relate modern coexistence theory to phylogenetic community assembly approaches to refine expectations for how species relatedness influences the outcome of competition. We argue that two types of species differences determine competitive exclusion with opposing effects on relatedness patterns. Importantly, this means that competition can sometimes eliminate more different and less related taxa, even when the traits underlying the relevant species differences are phylogenetically conserved. Our argument leads to a reinterpretation of the assembly processes inferred from community phylogenetic structure.
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            Stress tolerance in plants via habitat-adapted symbiosis.

            We demonstrate that native grass species from coastal and geothermal habitats require symbiotic fungal endophytes for salt and heat tolerance, respectively. Symbiotically conferred stress tolerance is a habitat-specific phenomenon with geothermal endophytes conferring heat but not salt tolerance, and coastal endophytes conferring salt but not heat tolerance. The same fungal species isolated from plants in habitats devoid of salt or heat stress did not confer these stress tolerances. Moreover, fungal endophytes from agricultural crops conferred disease resistance and not salt or heat tolerance. We define habitat-specific, symbiotically-conferred stress tolerance as habitat-adapted symbiosis and hypothesize that it is responsible for the establishment of plants in high-stress habitats. The agricultural, coastal and geothermal plant endophytes also colonized tomato (a model eudicot) and conferred disease, salt and heat tolerance, respectively. In addition, the coastal plant endophyte colonized rice (a model monocot) and conferred salt tolerance. These endophytes have a broad host range encompassing both monocots and eudicots. Interestingly, the endophytes also conferred drought tolerance to plants regardless of the habitat of origin. Abiotic stress tolerance correlated either with a decrease in water consumption or reactive oxygen sensitivity/generation but not to increased osmolyte production. The ability of fungal endophytes to confer stress tolerance to plants may provide a novel strategy for mitigating the impacts of global climate change on agricultural and native plant communities.
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              Responses of soil bacterial and fungal communities to extreme desiccation and rewetting.

              The microbial response to summer desiccation reflects adaptation strategies, setting the stage for a large rainfall-induced soil CO2 pulse upon rewetting, an important component of the ecosystem carbon budget. In three California annual grasslands, the present (DNA-based) and potentially active (RNA-based) soil bacterial and fungal communities were tracked over a summer season and in response to controlled rewetting of intact soil cores. Phylogenetic marker genes for bacterial (16S) and fungal (28S) RNA and DNA were sequenced, and the abundances of these genes and transcripts were measured. Although bacterial community composition differed among sites, all sites shared a similar response pattern of the present and potentially active bacterial community to dry-down and wet-up. In contrast, the fungal community was not detectably different among sites, and was largely unaffected by dry-down, showing marked resistance to dessication. The potentially active bacterial community changed significantly as summer dry-down progressed, then returned to pre-dry-down composition within several hours of rewetting, displaying spectacular resilience. Upon rewetting, transcript copies of bacterial rpoB genes increased consistently, reflecting rapid activity resumption. Acidobacteria and Actinobacteria were the most abundant phyla present and potentially active, and showed the largest changes in relative abundance. The relative increase (Actinobacteria) and decrease (Acidobacteria) with dry-down, and the reverse responses to rewetting reflected a differential response, which was conserved at the phylum level and consistent across sites. These contrasting desiccation-related bacterial life-strategies suggest that predicted changes in precipitation patterns may affect soil nutrient and carbon cycling by differentially impacting activity patterns of microbial communities.

                Author and article information

                Contributors
                clumibao@alumni.nd.edu
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                19 October 2019
                November 2019
                : 9
                : 21 ( doiID: 10.1002/ece3.v9.21 )
                : 12231-12244
                Affiliations
                [ 1 ] Department of Ecology, Evolution and Behavior University of Minnesota St. Paul Minnesota
                [ 2 ] Department of Plant Pathology University of Minnesota St. Paul Minnesota
                Author notes
                [*] [* ] Correspondence

                Candice Y. Lumibao, Department of Ecology and Evolutionary Biology, University of Tennessee Knoxville, 569 Dabney Hall, Knoxville, TN 37916.

                Email: clumibao@ 123456alumni.nd.edu

                Author information
                https://orcid.org/0000-0002-1414-7949
                https://orcid.org/0000-0001-6780-9259
                Article
                ECE35711
                10.1002/ece3.5711
                6854330
                31832156
                8422c59f-9657-4ae7-907c-086d5bceae9d
                © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 17 January 2019
                : 04 September 2019
                : 06 September 2019
                Page count
                Figures: 6, Tables: 2, Pages: 14, Words: 10189
                Funding
                Funded by: National Science Foundation , open-funder-registry 10.13039/100000001;
                Award ID: EF 12‐ 41895
                Award ID: DEB‐1556649
                Funded by: National Science Foundation Research Coordination Network
                Award ID: NSF‐DEB‐1042132
                Funded by: Long Term Ecological Research
                Award ID: NSF‐DEB‐1234162
                Funded by: Institute on the Environment
                Award ID: DG‐0001‐13
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                November 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.1 mode:remove_FC converted:14.11.2019

                Evolutionary Biology
                andropogon gerardii,nitrogen, phosphorus, potassium,nutrient network,phylogenetic diversity,plant fungal endophytes,spatial variation

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