Abstract
Soil microbial communities can have an important role in the adaptation of plants to their local abiotic soil conditions and in mediating plant responses to environmental stress. This has been clearly demonstrated for individual plant species, but it is unknown how locally adapted microbes may affect plant communities. It is possible that the adaptation of microbial communities to local conditions can shape plant community composition. Additionally, it is possible that the effects of locally adapted microorganisms on individual plant species could be altered by co-occurring plant species. We tested these possibilities in plant community mesocosms with soils and mycorrhizal fungi (AMF) from three locations. We found that plant community biomass responded positively to local adaptation of AMF to soil conditions. Plant community composition also changed in response to local adaptation of AMF. Unexpectedly, the strongest benefits of locally adapted AMF went to early successional plant species that have the highest relative growth rates and the lowest responsiveness to the presence of AMF. Late successional plants that responded positively overall to the presence of AMF were often suppressed in communities with local AMF, perhaps because of strong competition from fast growing plant species. These results show that local adaptation of soil microbial communities can shape plant community composition, and the benefits that plants derive from locally adapted microorganisms can be reshaped by the competitive context in which these associations occur.
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References
Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42. https://doi.org/10.1007/s005720100097
Barrett LG, Broadhurst LM, Thrall PH (2012) Geographic adaptation in plant-soil mutualisms: tests using Acacia spp. and rhizobial bacteria. Funct Ecol 26:457–468. https://doi.org/10.1111/j.1365-2435.2011.01940.x
Bauer JT, Kleczewski NM, Bever JD, Clay K, Reynolds HL (2012) Nitrogen-fixing bacteria, arbuscular mycorrhizal fungi, and the productivity and structure of prairie grassland communities. Oecologia 170:1089–1098. https://doi.org/10.1007/s00442-012-2363-3
Bauer JT, Blumenthal N, Miller AJ, Ferguson JK, Reynolds HL (2017) Effects of between-site variation in soil microbial communities and plant-soil feedbacks on the productivity and composition of plant communities. J Appl Ecol 54:1028–1039. https://doi.org/10.1111/1365-2664.12937
Bauer JT, Koziol L, Bever JD (2018) Ecology of floristic quality assessment: testing for correlations between coefficients of conservatism, species traits and mycorrhizal responsiveness. AoB Plants. https://doi.org/10.1093/aobpla/plx073
Blanquart F, Kaltz O, Nuismer SL, Gandon S (2013) A practical guide to measuring local adaptation. Ecol Lett 16:1195–1205. https://doi.org/10.1111/ele.12150
Delavaux CS, Smith-Ramesh LM, Kuebbing SE (2017) Beyond nutrients: a meta-analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology 98:2111–2119. https://doi.org/10.1002/ecy.1892
Fay PA, Carlisle JD, Knapp AK, Blair JM, Collins SL (2003) Productivity responses to altered rainfall patterns in a C 4-dominated grassland. Oecologia 137:245–251. https://doi.org/10.1007/s00442-003-1331-3
Harris J (2009) Soil microbial communities and restoration ecology: facilitators or followers? Science 325:573–574. https://doi.org/10.1126/science.1172975
Hartnett DC, Wilson GWT (1999) Mycorrhizae influence plant community structure and diversity in tallgrass prairie. Ecology 80:1187–1195
Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci 107:2093–2098. https://doi.org/10.1073/pnas.0906710107
Knapp AK, Briggs JM, Koelliker JK (2001) Frequency and extent of water limitation to primary production in a mesic temperate grassland. Ecosystems 4:19–28. https://doi.org/10.1007/s100210000057
Koziol L, Bever JD (2015) Mycorrhizal response trades off with plant growth rate and increases with plant successional status. Ecology 96:1768–1774. https://doi.org/10.1890/14-2208.1
Koziol L, Bever JD (2016) AMF, phylogeny, and succession: specificity of response to mycorrhizal fungi increases for late-successional plants. Ecosphere 7:e01555. https://doi.org/10.1002/ecs2.1555
Koziol L, Bever JD (2017) The missing link in grassland restoration: arbuscular mycorrhizal fungi inoculation increases plant diversity and accelerates succession. J Appl Ecol 54:1301–1309. https://doi.org/10.1111/1365-2664.12843
Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci 109:14058–14062. https://doi.org/10.1073/pnas.1202319109
Middleton EL, Bever JD (2012) Inoculation with a native soil community advances succession in a grassland restoration. Restor Ecol 20:218–226. https://doi.org/10.1111/j.1526-100X.2010.00752.x
Middleton EL, Richardson S, Koziol L, Palmer CE, Yermakov Z, Henning JA, Schultz PA, Bever JD (2015) Locally-adapted arbuscular mycorrhizal fungi improve vigor and resistance to herbivory of native prairie plant species. Ecosphere 6:276. https://doi.org/10.1890/ES15-00152.1
Reynolds HL, Packer A, Bever JD, Clay K (2003) Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291. https://doi.org/10.1890/02-0298
Rúa MA, Antoninka A, Antunes PM, Chaudhary VB, Gehring C, Lamit LJ, Piculell BJ, Bever JD, Zabinski C, Meadow JF, Lajeunesse MJ, Milligan BG, Karst J, Hoeksema JD (2016) Home-field advantage? Evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis. BMC Evol Biol 16:122. https://doi.org/10.1186/s12862-016-0698-9
Sanford WE, Selnick DL (2013) Estimation of evapotranspiration across the conterminous united states using a regression with climate and land-cover data1. J Am Water Resour Assoc 49:217–230. https://doi.org/10.1111/jawr.12010
Schultz PA, Miller RM, Jastrow JD, Rivetta CV, Bever JD (2001) Evidence of a mycorrhizal mechanism for the adaptation of Andropogon gerardii (Poaceae) to high- and low-nutrient prairies. Am J Bot 88:1650. https://doi.org/10.2307/3558410
Sherrard ME, Maherali H (2012) Local adaptation across a fertility gradient is influenced by soil biota in the invasive grass, Bromus inermis. Evol Ecol 26:529–544. https://doi.org/10.1007/s10682-011-9518-2
Stahl PD, Smith WK (1984) Effects of different geographic isolates of Glomus on the water relations of Agropyron smithii. Mycologia 76:261–267. https://doi.org/10.1080/00275514.1984.12023835
Thrall PH, Burdon JJ, Bever JD (2002) Local adaptation in the Linum marginale Melampsora lini host-pathogen interaction. Evolution 56:1340–1351. https://doi.org/10.1111/j.0014-3820.2002.tb01448.x
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72. https://doi.org/10.1038/23932
Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of the tallgrass prairie system. New Phytol 172:554–562. https://doi.org/10.1111/j.1469-8137.2006.01854.x
Wilson GWT, Hartnett DC (1998) Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am J Bot 85:1732–1738. https://doi.org/10.2307/2446507
Acknowledgements
This work was supported by Strategic Environmental Research and Development Program grant RC-2330 and National Science Foundation grants 1556664 and 1656006 to JDB and United States Department of Agriculture–National Institute of Food and Agriculture Grant 2016-67012-24680 to JTB. We appreciate assistance with greenhouse work from Ying “Bank” Xuen Hoe, Vanessa Snyder, and Alex Varney.
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JTB, LK, and JDB designed the experiment. JTB and LK established the experiment. JTB collected and analyzed data. JTB wrote the manuscript, with feedback and revisions from LK and JDB.
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Liz Koziol is the owner of Mycobloom LLC.
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Communicated by Sarah M. Emery.
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Bauer, J.T., Koziol, L. & Bever, J.D. Local adaptation of mycorrhizae communities changes plant community composition and increases aboveground productivity. Oecologia 192, 735–744 (2020). https://doi.org/10.1007/s00442-020-04598-9
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DOI: https://doi.org/10.1007/s00442-020-04598-9