Skip to main content
SpringerLink
Log in

Crop rotation reduces the frequency of anaerobic soil bacteria in Red Latosol of Brazil

  • Environmental Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Crop diversity affects the processes of soil physical structuring and most likely provokes changes in the frequencies of soil microbial communities. The study was conducted for soil prokaryotic diversity sequencing 16S rDNA genes from a 25-year no-tillage experiment comprised of two crop systems: crop succession (Triticum aestivum-Glycine max) and rotation (Vicia sativa-Zea mays-Avena sativa-Glycine max-Triticum aestivum-Glycine max). The hypothesis was that a crop system with higher crop diversification (rotation) would affect the frequencies of prokaryotic taxa against a less diverse crop system (succession) altering the major soil functions guided by bacterial diversity. Soils in both crop systems were dominated by Proteobacteria (31%), Acidobacteria (23%), Actinobacteria (10%), and Gemmatimonadetes (7.2%), among other common copiotrophic soil bacteria. Crop systems did not affect the richness and diversity indexes of soil bacteria and soil archaea. However, the crop rotation system reduced only the frequencies of anaerobic metabolism bacteria Chloroacidobacteria, Holophagae, Spirochaetes, Euryarchaeota, and Crenarchaeota. It can be concluded that crop succession, a system that is poorer in root diversity over time, may have conditioned the soil to lower oxygen diffusion and built up ecological niches that suitable for anaerobic bacteria tolerating lower levels of oxygen. On the other hand, it appeared that crop rotation has restructured the soil over the years while enabling copiotrophic aerobic bacteria to dominate the soil ecosystem. The changes prompted by crop succession have implications for efficient soil organic matter decomposition, reduced greenhouse gas emissions, higher root activity, and overall soil productivity, which compromise to agriculture sustainability.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Anzalone RA, Vezzani FM, Kaschuk G, Hungria M, Vargas LK, Nogueira MA (2020) Establishing reference values for soil microbial biomass-C in agroecosystems in the Atlantic Forest Biome in Southern Brazil. Ecol Indic 117:106586. https://doi.org/10.1016/j.ecolind.2020.106586

    Article  CAS  Google Scholar 

  2. Hooper DU, Bignell DE, Brown VK, Brussard L, Dangerfield JM, 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: We assess the evidence for correlation between aboveground and belowground diversity and conclude that a variety of mechanisms could lead to positive, negative, or no relationship—depending on the strength and type of interactions among species. Bioscience 50:1049–1061. https://doi.org/10.1641/0006-3568(2000)050[1049:IBAABB]2.0.CO;2

    Article  Google Scholar 

  3. Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8:1577–1587. https://doi.org/10.1038/ismej.2014.17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Tiemann LK, Grandy AS, Atkinson EE, Marin-Spiotta E, McDaniel MD (2015) Crop rotational diversity enhances belowground communities and functions in an agroecosystem. Ecol Lett 18:761–771. https://doi.org/10.1111/ele.12453

    Article  CAS  PubMed  Google Scholar 

  5. Eisenhauer N (2016) Plant diversity effects on soil microorganisms: spatial and temporal heterogeneity of plant inputs increase soil biodiversity. Pedobiologia 59:175–177. https://doi.org/10.1016/j.pedobi.2016.04.004

    Article  Google Scholar 

  6. Eisenhauer N, Lanoue A, Strecker T, Scheu S, Steinauer K, Thakur MP, Mommer L (2017) Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Sci Rep 7:44641. https://doi.org/10.1038/srep44641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Peralta AL, Sun Y, McDaniel MD, Lennon JT (2018) Crop rotational diversity increases disease suppressive capacity of soil microbiomes. Ecosphere 9:e02235. https://doi.org/10.1002/ecs2.2235

    Article  Google Scholar 

  8. McDaniel MD, Tiemann LK, Grandy AS (2014) Does agricultural crop diversity enhances soil microbial biomass and organic matter dynamics? A meta-analysis. Ecol Appl 24:560–570. https://doi.org/10.1890/13-0616.1

    Article  CAS  PubMed  Google Scholar 

  9. Venter ZS, Karin J, Heidi-Jayne H (2016) The impact of crop rotation on soil microbial diversity: a meta-analysis. Pedobiolgia 59(4):215–223. https://doi.org/10.1016/j.pedobi.2016.04.001

    Article  Google Scholar 

  10. Kaschuk G, Alberton O, Hungria M (2010) Three decades of soil microbial biomass studies in Brazilian ecosystems: lessons learned about soil quality and indications for improving sustainability. Soil Biol Biochem 42:1–10. https://doi.org/10.1016/j.soilbio.2009.08.020

    Article  CAS  Google Scholar 

  11. Alvares CA, Stape JL, Sentelhas PC, Gonçalves JL, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Zeitschrift 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507

    Article  Google Scholar 

  12. Santos HG, Jacomine PKT, Anjos LHC, Oliveira VA, Lumbreras JF, Coelho MR, Almeida JA, Araújo-Filho JC, Oliveira JB, Cunha TJF (2018) Brazilian soil classification system. 5th edn. Rev. and Exp. Embrapa, Brasília, 2018

  13. Pauletti V, Motta ACV (2019) Manual de Adubação e Calagem para o Estado do Paraná (2ª ed) Sociedade Brasileira de Ciência do Solo - Núcleo Estadual Paraná. Curitiba, pp 289

  14. Gee GW, Bauder JW (1986) Particle-size analysis. In: Klute A (ed.) Methods of soil analysis. Part 1. 2nd edn. Agron. Monogr. 9. ASA and SSSA. Madison, 383–411

  15. RStudio Team (2016) RStudio: integrated development for R. RStudio. Inc.. Boston. MA. http://www.rstudio.com/. Accessed 23 June 2016

  16. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. https://doi.org/10.1038/ismej.2012.8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596. https://doi.org/10.1093/nar/gks1219

    Article  CAS  Google Scholar 

  18. Jia Y, Whalen JK (2020) A new perspective on functional redundancy and phylogenetic niche conservatism in soil microbial communities. Pedosphere 30:18–24. https://doi.org/10.1016/S1002-0160(19)60826-X

    Article  Google Scholar 

  19. Souza RC, Cantão ME, Vasconcelos ATR, Nogueira MA, Hungria M (2013) Soil metagenomics reveals differences under conventional and no-tillage with crop rotation or succession. Appl Soil Ecol 72:49–61. https://doi.org/10.1016/j.apsoil.2013.05.021

    Article  Google Scholar 

  20. Souza RC, Mendes IC, Reis-Junior FB, Carvalho FM, Nogueira MA, Vasconcelos ATR, Vicente VA, Hungria M (2016) Shifts in taxonomic and functional microbial diversity with agriculture: how fragile is the Brazilian Cerrado? BMC Microbiol 16:42. https://doi.org/10.1186/s12866-016-0657-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. 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(11):e51075. https://doi.org/10.1371/journal.pone.0051075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ashworth AJ, De Bruyn JM, Allen FL, Radosevich M, Owens PR (2017) Microbial community structure is affected by cropping sequences and poultry litter under long-term no-tillage. Soil Biol Biochem 114:210–219. https://doi.org/10.1016/j.soilbio.2017.07.019

    Article  CAS  Google Scholar 

  23. Babin D, Deubel A, Jacquiod S, Sørensen SJ, Geistlinger J, Grosch R, Smalla K (2019) Impact of long-term agricultural management practices on soil prokaryotic communities. Soil Biol Biochem 129:17–28. https://doi.org/10.1016/j.soilbio.2018.11.002

    Article  CAS  Google Scholar 

  24. Xia X, Zhang P, He L, Gao X, Li W, Zhou Y, Li Z, Li H, Yang L (2019) Effects of tillage managements and maize straw returning on soil microbiome using 16S rDNA sequencing. J Int Plant Biol 61:765–777. https://doi.org/10.1111/jipb.12802

    Article  CAS  Google Scholar 

  25. Carciochi WD, Rosso LHM, Secchi MA, Torres AR, Naeve S, Casteel SN, Kovács P, Davidson D, Purcell LC, Archontoulis S, Ciampitti IA (2019) Soybean yield, biological N2 fixation and seed composition responses to additional inoculation in the United States. Sci Rep 9:19908. https://doi.org/10.1038/s41598-019-56465-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Glick BR (2012)Plant growth-promoting bacteria: mechanisms and applications. Scientifica 963401. https://doi.org/10.6064/2012/963401

  27. Ferreira CMH, Soares HMVM, Soares EV (2019) Promising bacterial genera for agricultural practices: an insight on plant growth-promoting properties and microbial safety aspects. Sci Total Environ 682:779–799. https://doi.org/10.1016/j.scitotenv.2019.04.225

    Article  CAS  PubMed  Google Scholar 

  28. Aislabie J, Deslippe JR (2013) Soil microbes and their contribution to soil services. In: Dymond JR (ed) Ecosystem services in New Zealand-conditions and trends, pp 143–161

  29. Maron P-A, Sarr A, Kaisermann A, Lévêque J, Mathieu O, Guigue J, Karimi B, Bernard L, Dequiedt S, Terrat S, Chabbi A, Ranjard L (2018) High microbial diversity promotes soil ecosystem functioning. Appl Environm Microbiol 84(9):e02738-e2817. https://doi.org/10.1128/AEM.02738-17

    Article  CAS  Google Scholar 

  30. Ho A, Di Lonardo DP, Bodelier PLE (2017) Revisiting life strategy concepts in environmental microbial ecology. FEMS Microbiol Ecol 93:fix006. https://doi.org/10.1093/femsec/fix006

    Article  CAS  Google Scholar 

  31. Eichorst SA, Trojan D, Roux S, Herbold C, Rattei T, Woebken D (2018) Genomic insights into the Acidobacteria reveal strategies for their success in terrestrial environments. Environ Microbiol 20:1041–1063. https://doi.org/10.1111/1462-2920.14043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Tank M, Bryant DA (2015) Chloracidobacterium thermophilum gen. nov. sp. nov.: an anoxygenic microaerophilic chlorophotoheterotrophic acidobacterium. Int J Syst Evol Microbiol 65:1426–1430. https://doi.org/10.1099/ijs.0.000113

    Article  CAS  PubMed  Google Scholar 

  33. Liesack W, Bak F, Kreft JU, Stackebrandt E (1994) Holophaga foetida gen. nov. sp. nov. a new. homoacetogenic bacterium degrading methoxylated aromatic compounds. Arch Microbiol 162:85–90

    CAS  PubMed  Google Scholar 

  34. Nunes da Rocha U, Plugge CM, George I, van Elsas JD, van Overbeek LS (2013) The rhizosphere selects for particular groups of Acidobacteria and Verrucomicrobia. PLoS ONE 8(12):e82443. https://doi.org/10.1371/journal.pone.0082443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Anderson I, Held B, Lapidus A, Nolan M, Lucas S, Tice H, Del Rio TG, Cheng JF, Han C, Tapia R, Goodwin LA, Pitluck S, Liolios K, Mavromatis K, Pagani I, Ivanova N, Mikhailova N, Pati A, Chen A, Palaniappan K, Land M, Brambilla EM, Rohde M, Spring S, Göker M, Detter JC, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Klenk HP, Kyrpides NC (2012) Genome sequence of the homoacetogenic bacterium Holophaga foetida type strain (TMBS4(T)). Stand Genomic Sci 6:174–84. https://doi.org/10.4056/sigs.2746047

    Article  PubMed  PubMed Central  Google Scholar 

  36. Dong X, Greening C, Brüls T, Conrad R, Guo K, Blaskowski S, Kaschani F, Kaiser M, Laban NA, Meckenstock RU (2018) Fermentative Spirochaetes mediate necromass recycling in anoxic hydrocarbon-contaminated habitats. ISME J 12:2039–2050. https://doi.org/10.1038/s41396-018-0148-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Kessler AJ, Chen Y, Waite DW, Hutchinson T, Koh S, Popa ME, Beardall J, Hugenholtz P, Cook PLM, Greening C (2019) Bacterial fermentation and respiration processes are uncoupled in anoxic permeable sediments. Nat Microbiol 4:1014–1023. https://doi.org/10.1038/s41564-019-0391-z

    Article  CAS  PubMed  Google Scholar 

  38. Greening C, Grinter R, Chiri E (2019) Uncovering the metabolic strategies of the dormant microbial majority: towards integrative approaches. mSystems 4:e00107-19. https://doi.org/10.1128/mSystems.00107-19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Timonen S, Bomberg M (2009) Archaea in dry soil environments. Phytochem Rev 8:505–518. https://doi.org/10.1007/s11101-009-9137-5

    Article  CAS  Google Scholar 

  40. Schmidt R, Gravuer K, Bossange AV, Mitchell J, Scow K (2018) Long-term use of cover crops and no-till shift soil microbial community life strategies in agricultural soil. PLoS ONE 13(2):e0192953. https://doi.org/10.1371/journal.pone.0192953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Stahl DA, de la Torre JR (2013) Physiology and diversity of ammonia-oxidizing Archaea. Ann Rev Microbiol 66:83–101. https://doi.org/10.1146/annurev-micro-092611-150128

    Article  CAS  Google Scholar 

  42. Vezzani FM, Graig A, Meenken E, Gillespie R, Peterson M, Beare MH (2018) The importance of plants to development and maintenance of soil structure, microbial communities and ecosystem functions. Soil Til Res 175:139–149. https://doi.org/10.1016/j.still.2017.09.002

    Article  Google Scholar 

  43. Gamboa CH, Vezzani FM, Kaschuk G, Favaretto N, Cobos JYG, Costa GA (2020) Soil-Root Dynamics in maize-beans-eggplant intercropping system under organic management in a Subtropical Region. J Soil Sci Plant Nutr. https://doi.org/10.1007/s42729-020-00227-9

    Article  Google Scholar 

  44. Rasse DP, Rumpel C, Dignac M (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–356. https://doi.org/10.1007/s11104-004-0907-y

    Article  CAS  Google Scholar 

  45. Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept and review. Soil Biol Biochem 83:184–199. https://doi.org/10.1016/j.soilbio.2015.01.025

    Article  CAS  Google Scholar 

  46. Behnke GD, Villamil MB (2019) Cover crop rotations affect greenhouse gas emissions and crop production in Illinois, USA. Field Crop Res 241:107580. https://doi.org/10.1016/j.fcr.2019.107580

    Article  Google Scholar 

  47. Rosenberg E (2014) The Phylum Fibrobacteres. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Springer, Berlin, Heidelberg

    Google Scholar 

  48. Fedosov DV, Podkopaeva DA, Miroshnichenko ML, Bonch-Osmolovskaya EA, Lebedinsky AV, Grabovich MY (2006) Investigation of the catabolism of acetate and peptides in the new anaerobic thermophilic bacterium Caldithrix abyssi. Microbiology 75:119–212. https://doi.org/10.1134/S0026261706020020

    Article  CAS  Google Scholar 

  49. Timmers PHA, Welte CU, Koehorst JJ, Plugge CM, Jetten MSM, Stams AJM (2017) Reverse methanogenesis and respiration in Methanotrophic Archaea. Archaea 2017:1654237. https://doi.org/10.1155/2017/1654237

Download references

Acknowledgements

The authors acknowledge the Foundation ABC for allowing the collection of soil samples in their long-term experiment; the Federal University of Paraná’s Graduate Support Program (PROAP, for its acronym in Portuguese) in Curitiba, Brazil; the Brazilian Council for Scientific and Technological Development (CNPq) for financing this work; Carla Gomes Albuquerque, Denise de Conti, Fabiana Gavelaki, Heila Silva Araújo, Josianne Meyer, Leticia Maduro Gonçalves, Maria Aparecida Carvalho Santos, and Marla Cristina Becker Motta for their technical assistance; and Veridiana Cherobim for her helping hand in soil sampling. Raul Matias Cezar acknowledges the Coordination of Improvement of Higher Education Personnel (CAPES, Brazil) for the scholarship.

Funding

This study was funded by the Graduate Support Program (PROAP) of the Federal University of Paraná, Brazil, and the Brazilian Council for Scientific and Technological Development (CNPq).

Author information

Authors and Affiliations

  1. Post-Graduate in Soil Science, Federal University of Paraná, Rua Dos Funcionários, 1540, Curitiba, PR, CEP 80035-050, Brazil

    Raul Matias Cezar, Fabiane Machado Vezzani & Glaciela Kaschuk

  2. Department of Biochemistry, Federal University of Paraná, Rua Francisco H. Dos Santos S/N, Curitiba, PR, CEP 81531-990, Brazil

    Eduardo Balsanelli & Emanuel Maltempi de Souza

  3. Department of Agricultural Diagnosis and Research, Secretary of Agriculture and Livestock of the State of Rio Grande Do Sul, Rua Gonçalves Dias, 570, Porto Alegre, RS, CEP 90130-060, Brazil

    Luciano Kayser Vargas

  4. ABC Foundation, Rod. PR 151 km 288, Caixa-postal: 1003, Castro, PR, CEP 84165-700, Brazil

    Rudimar Molin

Authors
  1. Raul Matias Cezar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fabiane Machado Vezzani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Glaciela Kaschuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eduardo Balsanelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Emanuel Maltempi de Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Luciano Kayser Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rudimar Molin
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Raul Matias Cezar took the leadership in the conductance of the work. All authors have contributed in the steps of conception and design of the work, acquisition, analysis, and interpretation of data. All authors contributed in the draft and the critical revision of the work. All authors have approved the version to be published and have agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Corresponding author

Correspondence to Glaciela Kaschuk.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Highlights

• Crop rotation provokes changes in the frequencies of the soil 16S rDNA gene.

• Chloroacidobacteria increases in the soil under crop rotation systems.

• Holophagae, Spirochaetes, Euryarchaeota, and Crenarchaeota were suppressed in crop rotation.

• 16S rDNA sequencing depicts changes in soil microbial community structure.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cezar, R.M., Vezzani, F.M., Kaschuk, G. et al. Crop rotation reduces the frequency of anaerobic soil bacteria in Red Latosol of Brazil. Braz J Microbiol 52, 2169–2177 (2021). https://doi.org/10.1007/s42770-021-00578-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-021-00578-0

Keywords

Search

Navigation