Abstract
Old fields are spreading in the world because of agriculture abandonment, and they show a persistence of exotic plant species with little recovery towards the original vegetation composition. Soil biota may also differ between old fields and native grasslands, but were comparatively less studied than plant communities, despite their importance in biogeochemical processes. Here we compared soil bacterial communities of exotic-dominated old fields with those of remnants of native grasslands in the Inland Pampa, Argentina, using the 16S rRNA gene amplicon sequencing approach. We also characterized plant communities, soil physico-chemical properties, and soil respiration. We expected more diverse soil bacterial communities, with higher heterogeneity, in remnant grasslands than in old fields because of a more diverse and more heterogeneous plant community. However, our results showed that soil bacterial communities had higher Shannon diversity in old fields than in remnant grasslands, but richness was not significantly different. Also we found different bacterial community compositions between grasslands even at a low taxonomic level. On the other hand, old fields harbored less heterogeneous bacterial communities than remnants, and bacteria and plant beta diversity were correlated. Despite contrasting plant and bacterial composition between old fields and remnant grasslands, soil physico-chemical properties were quite similar between grasslands. Overall, our results showed that bacterial communities in grassland soils were associated with changes in plant communities after agricultural abandonment. Plant-microbial feedbacks might regulate plant and soil bacterial community assemblage in old fields, yet further research is needed to demonstrate this potential feedback mechanism.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Baldi G, Guerschman JP, Paruelo JM (2006) Characterizing fragmentation in temperate South America grasslands. Agric Ecosyst Environ 116:197–208. https://doi.org/10.1016/j.agee.2006.02.009
Bergmann GT, Bates ST, Eilers KG, Lauber CL, Caporaso JG, Walters WA, Knight R, Fierer N (2011) The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biol Biochem 43:1450–1455. https://doi.org/10.1016/j.soilbio.2011.03.012
Bodelier PLE (2011) Toward understanding, managing, and protecting microbial ecosystems. Front Microbiol 2:1–8. https://doi.org/10.3389/fmicb.2011.00080
Bowles TM, Acosta-Martínez V, Calderón F, Jackson LE (2014) Soil enzyme activities, microbial communities, and carbon and nitrogen availability in organic agroecosystems across an intensively-managed agricultural landscape. Soil Biol Biochem 68:252–262. https://doi.org/10.1016/j.soilbio.2013.10.004
Bray JR, Curtis JT (1957) An ordination of the upland forest communities of Southern Wisconsin. Ecol Monogr 27:325–349. https://doi.org/10.2307/1942268
Bray R, Kurtz L (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59(1):39–46
Burkart S, León R, Conde M, Perelman S (2011) Plant species diversity in remnant grasslands on arable soils in the cropping Pampa. Plant Ecol 212:1009–1024. https://doi.org/10.1007/s11258-010-9881-z
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R, Caporaso et al JG (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Meth 7:335–336. https://www.nature.com/nmeth/journal/v7/n5/suppinfo/nmeth.f.303_S1.html
Carbonetto B, Rascovan N, Alvarez R, Mentaberry A, Vázquez MP (2014) Structure, composition and metagenomic profile of soil microbiomes associated to agricultural land use and tillage systems in argentine pampas. PLoS ONE 9:e99949. https://doi.org/10.1371/journal.pone.0099949
Carvalhais LC, Dennis PG, Tyson GW, Schenk PM (2012) Application of metatranscriptomics to soil environments. J Microbiol Methods 91:246–251. https://doi.org/10.1016/j.mimet.2012.08.011
Compant S, Samad A, Faist H, Sessitsch A (2019) A review on the plant microbiome: ecology, functions, and emerging trends in microbial application. J Adv Res 19:29–37. https://doi.org/10.1016/j.jare.2019.03.004
Cramer VA, Hobbs RJ, Standish RJ (2008) What’s new about old fields? Land abandonment and ecosystem assembly. Trends Ecol Evol 23:104–112. https://doi.org/10.1016/j.tree.2007.10.005
da Jesus CE, Marsh TL, Tiedje JM, de Moreira FM (2009) Changes in land use alter the structure of bacterial communities in Western Amazon soils. ISME J 3:1004–1011. https://doi.org/10.1038/ismej.2009.98
Delgado-Baquerizo M, Oliverio AM, Brewer TE, Benavent-gonzález A, Eldridge DJ, Bardgett RD, Maestre FT, Singh BK, Fierer N (2018) A global atlas of the dominant bacteria found in soil. Science 80(359):320–325. https://doi.org/10.1126/science.aap9516
Fierer N (2017) Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol 15:579–590. https://doi.org/10.1038/nrmicro.2017.87
Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631. https://doi.org/10.1073/pnas.0507535103
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364. https://doi.org/10.1890/05-1839
Fierer N, Ladau J, Clemente JC, Leff JW, Owens SM, Pollard KS, Knight R, Gilbert JA, McCulley RL (2013) Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the United States. Science 80(342):621–624. https://doi.org/10.1126/science.1243768
Figuerola ELM, Guerrero LD, Rosa SM, Simonetti L, Duval ME, Galantini JA, Bedano JC, Wall LG, Erijman L (2012) Bacterial indicator of agricultural management for soil under no-till crop production. PLoS ONE 7:e51075. https://doi.org/10.1371/journal.pone.0051075
Figuerola ELM, Guerrero LD, Türkowsky D, Wall LG, Erijman L (2014) Crop monoculture rather than agriculture reduces the spatial turnover of soil bacterial communities at a regional scale. Environ Microbiol. https://doi.org/10.1111/1462-2920.12497
Gilbert JA, Jansson JK, Knight R (2014) The earth microbiome project: successes and aspirations. BMC Biol 12:69. https://doi.org/10.1186/s12915-014-0069-1
Herzog S, Wemheuer F, Wemheuer B, Daniel R, van Mil S, Wernars K (2015) Effects of fertilization and sampling time on composition and diversity of entire and active bacterial communities in German Grassland soils. PLoS ONE 10:e0145575. https://doi.org/10.1371/journal.pone.0145575
Hooper DU, Bignell DE, Brown VK, Brussard L, Mark Dangerfield J, Wall DH, Wardle DA, Coleman DC, Giller KE, Lavelle P, Van Der Putten WH, De Ruiter PC, Rusek J, Silver WL, Tiedje JM, Wolters V (2000) Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks. Bioscience 50:1049. https://doi.org/10.1641/0006-3568(2000)050[1049:IBAABB]2.0.CO;2
Inderjit WH, der Putten H (2010) Impacts of soil microbial communities on exotic plant invasions. Trends Ecol Evol 25:512–519. https://doi.org/10.1016/j.tree.2010.06.006
Kjeldahl J (1883) Neue methode zur bestimmung des stickstoffs in organischen körpern. Zeitschrift für Anal Chemie 22:366–382
Li H, Xu Z, Yan Q, Yang S, van Nostrand JD, Wang Z, He Z, Zhou J, Jiang Y, Deng Y (2017) Soil microbial beta-diversity is linked with compositional variation in aboveground plant biomass in a semi-arid grassland. Plant Soil 1:1–16. https://doi.org/10.1007/s11104-017-3524-2
Liao C, Peng R, Luo Y, Zhou X, Wu X, Fang C, Chen J, Li B (2008) Altered ecosysetm carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–714. https://doi.org/10.1111/j.1469-8137.2007.02290.x
Lima-Mendez G, Faust K, Henry N, Decelle J, Colin S, Carcillo F, Chaffron S, Ignacio-Espinosa JC, Roux S, Vincent F, Bittner L, Darzi Y, Wang J, Audic S, Berline L, Bontempi G, Cabello AM, Coppola L, Cornejo-Castillo FM, Ovidio F, De Meester L, Ferrera I, Garet-Delmas M-J, Guidi L, Lara E, Pesant S, Royo-Llonch M, Salazar G, Sánchez P, Sebastian M, Souffreau C, Dimier C, Picheral M, Searson S, Kandels-Lewis S, Gorsky G, Not F, Ogata H, Speich S, Stemmann L, Weissenbach J, Wincker P, Acinas SG, Sunagawa S, Bork P, Sullivan MB, Karsenti E, Bowler C, de Vargas C, Raes J (2015) Determinants of community structure in the global plankton interactome. Science 80(348):126–173. https://doi.org/10.1126/science.1262073
Lynn TM, Liu Q, Hu Y, Yuan H, Wu X, Khai AA, Wu J, Ge T (2017) Influence of land use on bacterial and archaeal diversity and community structures in three natural ecosystems and one agricultural soil. Arch Microbiol 199:1–11. https://doi.org/10.1007/s00203-017-1347-4
Mariotte P, Mehrabi Z, Bezemer TM, De Deyn GB, Kulmatiski A, Drigo B, Veen GF, van der Heijden MGA, Kardol P (2017) Plant-soil feedback: bridging natural and agricultural sciences. Trends Ecol Evol. https://doi.org/10.1016/j.tree.2017.11.005
McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data : a comment on distance-based redundancy analysis. Ecology 82:290–297. https://doi.org/10.1890/0012-9658(2001)082[0290:FMMTCD]2.0.CO;2
Milchunas DG, Sala OE, Lauenroth WK (1988) A generalized model of the effects of grazing by large herbivores on grassland community structure. Am Nat 132:87–106. https://doi.org/10.1086/284839
Morales SE, Holben WE (2011) Linking bacterial identities and ecosystem processes: can “omic” analyses be more than the sum of their parts? FEMS Microbiol Ecol 75:2–16. https://doi.org/10.1111/j.1574-6941.2010.00938.x
Nemergut DR, Schmidt SK, Fukami T, O’Neill SP, Bilinski TM, Stanish LF, Knelman JE, Darcy JL, Lynch RC, Wickey P, Ferrenberg S (2013) Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev 77:342–356. https://doi.org/10.1128/MMBR.00051-12
Omacini M, Tognetti P, Trebino H (2005) Sucesión postagrícola en la Pampa Interior: invasión y dominancia de plantas exóticas durante los primeros 20 años. In: Oesterheld M, Aguiar MR, Ghersa CM, Paruelo JM (eds) La heterogeneidad de la vegetación de los agroecosistemas. Un homenaje a Rolando León. Editorial Facultad de Agronomía, UBA, pp 215–234
Parera P, Al E (2014) Indice de contribución a la conservación de Pastizales Naturales del Cono Sur. Una herramienta para incentivar a los productores rurales, Argentina
Prober SM, Leff JW, Bates ST, Borer ET, Firn J, Harpole WS, Lind EM, Seabloom EW, Adler PB, Bakker JD, Cleland EE, Decrappeo NM, Delorenze E, Hagenah N, Hautier Y, Hofmockel KS, Kirkman KP, Knops JMH, La Pierre KJ, Macdougall AS, Mcculley RL, Mitchell CE, Risch AC, Schuetz M, Stevens CJ, Williams RJ, Fierer N (2015) Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol Lett 18:85–95. https://doi.org/10.1111/ele.12381
Raes J, Bork P (2008) Molecular eco-systems biology: towards an understanding of community function. Nat Rev Microbiol 6:693–699. https://doi.org/10.1038/nrmicro1935
Rascovan N, Carbonetto B, Revale S, Reinert MD, Alvarez R, Godeas AM, Colombo R, Aguilar M, Novas MV, Iannone L, Zelada AM, Pardo A, Schrauf G, Mentaberry A, Vazquez MP (2013) The PAMPA datasets: a metagenomic survey of microbial communities in Argentinean pampean soils. Microbiome 1:1–6. https://doi.org/10.1186/2049-2618-1-21
Robertson GP, Coleman DC, Bledsoe CS, Sollins P (1999) Standard Soil Methods for Long-Term Ecological Research. Oxford University Press on Demand, Oxford
Rodrigues JLM, Pellizari VH, Mueller R, Baek K, Jesus EDC, Paula FS, Mirza B, Hamaoui GS, Tsai SM, Feigl B, Tiedje JM, Bohannan BJM, Nüsslein K (2013) Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proc Natl Acad Sci 110:988–993. https://doi.org/10.1073/pnas.1220608110
Rodrigues RR, Pineda RP, Barney JN, Nilsen ET, Barrett JE, Williams MA, Shinsky J, White T (2015) Plant invasions associated with change in root-zone microbial community structure and diversity. PLoS ONE 10:e0141424. https://doi.org/10.1371/journal.pone.0141424
Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351. https://doi.org/10.1038/ismej.2010.58
Schöler A, Jacquiod S, Vestergaard G, Schulz S, Schloter M (2017) Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol Fertil Soils 53:485–489. https://doi.org/10.1007/s00374-017-1205-1
Soriano A (1991) Rio de la Plata grasslands. In: Coupland RT (ed) Natural grasslands: Introduction and western hemisphere. Elsevier, Amsterdam, pp 367–408
Spirito F, Yahdjian L, Tognetti PM, Chaneton EJ (2014) Soil ecosystem function under native and exotic plant assemblages as alternative states of successional grasslands. Acta Oecologica 54:4–12. https://doi.org/10.1016/j.actao.2012.10.004
Strickland MS, Lauber CL, Fierer N (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451. https://doi.org/10.1890/08-0296.1
Suding KN, Gross KL, Houseman GR (2004) Alternative states and positive feedbacks in restoration ecology. Trends Ecol Evol 19:46–53. https://doi.org/10.1016/j.tree.2003.10.005
Tognetti PM, Chaneton EJ (2015) Community disassembly and invasion of remnant native grasslands under fluctuating resource supply. J Appl Ecol 52:119–128. https://doi.org/10.1111/1365-2664.12349
Tognetti PM, Chaneton EJ, Omacini M, Trebino HJ, León RJC (2010) Exotic vs. native plant dominance over 20years of old-field succession on set-aside farmland in Argentina. Biol Conserv 143:2494–2503. https://doi.org/10.1016/j.biocon.2010.06.016
Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI (2007) The Human microbiome project. Nature 449:804–810. https://doi.org/10.1038/nature06244
Vega E, Baldi G, Jobbágy EG, Paruelo J (2009) Land use change patterns in the Río de la Plata grasslands: the influence of phytogeographic and political boundaries. Agric Ecosyst Environ 134:287–292. https://doi.org/10.1016/j.agee.2009.07.011
Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart—how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484. https://doi.org/10.1007/s00374-017-1191-3
Vilardo G, Tognetti PM, González-Arzac A, Yahdjian L (2018) Soil arthropod composition differs between old-fields dominated by exotic plant species and remnant native grasslands. Acta Oecologica 91:57–64. https://doi.org/10.1016/j.actao.2018.06.003
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38
Wardle D (2006) The influence of biotic interactions on soil biodiversity. Ecol Lett 9:870–886. https://doi.org/10.1111/j.1461-0248.2006.00931.x
Wolfe BE, Klironomos JN (2005) Breaking new ground: soil communities and exotic plant invasion. Bioscience 55:477–487. https://doi.org/10.1641/0006-3568(2005)055[0477:BNGSCA]2.0.CO;2
Yahdjian L, Piñeiro G (2014) Balance de Carbono en pastizales pampeanos. In: Medina CP, Zubillaga M, Taboada MÁ (eds) Suelos, producción agropecuaria y cambio climático: avances en la Argentina. Ministerio de Agricultura Ganadería y Pesca de la Nación, Ciudad Autónoma de Buenos Aires
Yahdjian L, Gherardi L, Sala OE (2014) Grasses have larger response than shrubs to increased nitrogen availability: a fertilization experiment in the Patagonian steppe. J Arid Environ 102:17–20. https://doi.org/10.1016/j.jaridenv.2013.11.002
Yahdjian L, Tognetti PM, Chaneton EJ (2017) Plant functional composition affects soil processes in novel successional grasslands. Funct Ecol. https://doi.org/10.1111/1365-2435.12885
Acknowledgements
We are especially grateful to Pablo Montes for experimental set-up, soil properties, and for performing vegetation analysis, and to Marcelo Soria for his expert advice on bioinformatics. We thank people that collaborated in field sampling and the staff at Estancia San Claudio for logistic support. Sergio Velasco Ayuso gave insightful advices on statistical analyses and comments on the first draft. This work was supported by Universidad de Buenos Aires (UBACyT 20020130100423BA), Agencia Nacional de Promoción Científica y Tecnológica (PICT 2014-3026) and Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 112-2015- 0100709).
Author information
Authors and Affiliations
Contributions
LY and XLZ designed and performed the experiments in the field. LV and XLZ did molecular and bioinformatic analyses. XLZ lead the writing of the manuscript and LY and LV contributed critically to the drafts and gave final approval for publication.
Corresponding author
Ethics declarations
Conflicts of interest
The authors have no conflict of interest to declare.
Additional information
Communicated by Edith B. Allen.
López Zieher, X.M.; Vivanco, L.; Yahdjian, L., Soil bacterial communities of old fields and remnants of natural grasslands of the Inland Pampa, Buenos Aires, Argentina Metagenome, NCBI, SRA accession: SRP149369.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
López Zieher, X.M., Vivanco, L. & Yahdjian, L. Soil bacterial communities remain altered after 30 years of agriculture abandonment in Pampa grasslands. Oecologia 193, 959–968 (2020). https://doi.org/10.1007/s00442-020-04736-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-020-04736-3