Ecological Processes Shaping Bulk Soil and Rhizosphere Microbiome Assembly in a Long-Term Amazon Forest-to-Agriculture Conversion
- 335 Downloads
Forest-to-agriculture conversion has been identified as a major threat to soil biodiversity and soil processes resilience, although the consequences of long-term land use change to microbial community assembly and ecological processes have been often neglected. Here, we combined metagenomic approach with a large environmental dataset, to (i) identify the microbial assembly patterns and, (ii) to evaluate the ecological processes governing microbial assembly, in bulk soil and soybean rhizosphere, along a long-term forest-to-agriculture conversion chronosequence, in Eastern Amazon. We hypothesized that (i) microbial communities in bulk soil and rhizosphere have different assembly patterns and (ii) the weight of the four ecological processes governing assembly differs between bulk soil and rhizosphere and along the chronosequence in the same fraction. Community assembly in bulk soil fitted most the zero-sum multinomial (ZSM) neutral-based model, regardless of time. Low to intermediate dispersal was observed. Decreasing influence of abiotic factors was counterbalanced by increasing influence of biotic factors, as the chronosequence advanced. Undominated ecological processes of dispersal limitation and variable selection governing community assembly were observed in this soil fraction. For soybean rhizosphere, community assembly fitted most the lognormal niche-based model in all chronosequence areas. High dispersal and an increasing influence of abiotic factors coupled with a decreasing influence of biotic factors were found along the chronosequence. Thus, we found a dominant role of dispersal process governing microbial assembly with a secondary effect of homogeneous selection process, mainly driven by decreasing aluminum and increased cations saturation in soil solution, due to long-term no-till cropping. Together, our results indicate that long-term no-till lead community abundances in bulk soil to be in a transient and conditional state, while for soybean rhizosphere, community abundances reach a periodic and permanent distribution state. Dominant dispersal process in rhizosphere, coupled with homogeneous selection, brings evidences that soybean root system selects microbial taxa via trade-offs in order to keep functional resilience of soil processes.
KeywordsMetagenomics Microbial dispersal Neutral theory Selection Soybean rhizosphere
DG-S and SMT designed the project. DG-S collected the soil samples. DG-S conducted the experiment. DG-S and LWM performed the metagenome analyses. DG-S and LWM analyzed the metadata. DG-S, LWM, JLMR, and SMT wrote the manuscript.
This study was funded by the São Paulo Research Foundation (FAPESP/CNPq No. 2008/58114-3 and FAPESP/NSF No. 2014/50320-4). DG-S received a scholarship from National Council for Scientific and Technological Development (PRONEX-CNPq # 140317/2014-7). SMT thanks CNPq (CNPq-PQ 311008/2016-0).
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interest.
- 1.Rodrigues JLM, Pellizari VH, Mueller R, Baek K, Jesus EC, Paula FS, Mirza B, Hamaoui GS, Tsai SM, Feigl B, Tiedje JM, Bohannan BJM, Nusslein K (2013) Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proc. Natl. Acad. Sci. U. S. A. 110:988–993. https://doi.org/10.1073/pnas.1220608110 CrossRefPubMedGoogle Scholar
- 4.Smith CR, Blair PL, Boyd C, Cody B, Hazel A, Hedrick A, Kathuria H, Khurana P, Kramer B, Muterspaw K, Peck C, Sells E, Skinner J, Tegeler C, Wolfe Z (2016) Microbial community responses to soil tillage and crop rotation in a corn/soybean agroecosystem. Ecol Evol 6:8075–8084. https://doi.org/10.1002/ece3.2553 CrossRefPubMedPubMedCentralGoogle Scholar
- 10.Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. U. S. A. 108:4516–4522. https://doi.org/10.1073/pnas.1000080107 CrossRefPubMedGoogle Scholar
- 14.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 CrossRefPubMedPubMedCentralGoogle Scholar
- 23.Fan K, Cardona C, Li Y, Shi Y, Xiang X, Shen C, Wang H, Gilbert JA, Chu H (2017) Rhizosphere-associated bacterial network structure and spatial distribution differ significantly from bulk soil in wheat crop fields. Soil Biol. Biochem. 113:275–284. https://doi.org/10.1016/j.soilbio.2017.06.020 CrossRefGoogle Scholar
- 35.Gee GW, Bauder JW (1986) Particle-size analysis. In: Klute A (ed) Methods of soil analysis. ASA, Madison, pp 383–411Google Scholar
- 36.Tedesco MJ, Gianello C, Bissani CA et al (1995) Analysis of soil, plants and other materials. Universidade Federal do Rio Grande do Sul, Porto AlegreGoogle Scholar
- 37.Claessen MEC, Barreto WO, Paula JL, Duarte MN (1997) Manual of soil analysis methods2nd edn. Embrapa, Rio de JaneiroGoogle Scholar
- 39.Keeney DR, Nelson DW (1982) Nitrogen - inorganic forms. In: Page AL (ed) Methods in soil analysis, part 22nd edn. ASA and SSSA, Madison, pp 643–698Google Scholar
- 40.Melo WJ, Melo GMP, Araújo ASF, Melo VP (2010) Avaliação da atividade enzimática em amostras de solo. In: Figueiredo MVB, Burity HA, Oliveira JP, Santos CE (eds) Biotecnologia aplicada à agricultura. Embrapa, Recife, pp 153–187Google Scholar
- 42.Zhbannikov IY, Hunter SS, Foster JA et al (2017) SeqyClean: a pipeline for high-throughput sequence data preprocessing. In: ACM (ed) Proceedings of the 8th ACM international conference on bioinformatics, computational biology, and health informatics (ACM-BCB ‘17). ACM, Boston, pp 407–416Google Scholar
- 44.Wilke A, Harrison T, Wilkening J, Field D, Glass EM, Kyrpides N, Mavrommatis K, Meyer F (2012) The M5nr: a novel non-redundant database containing protein sequences and annotations from multiple sources and associated tools. BMC Bioinformatics 13:1–5. https://doi.org/10.1186/1471-2105-13-141 CrossRefGoogle Scholar
- 45.Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R (2013) The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res. 42:1–9. https://doi.org/10.1093/nar/gkt1226 CrossRefGoogle Scholar
- 53.Lepš J, Šmilauer P (2005) Multivariate analysis of ecological data using CANOCO. Bull. Ecol. Soc. Am. 86:6–6. https://doi.org/10.1890/0012-9623(2005)86[6a:MAOEDU]2.0.CO;2 CrossRefGoogle Scholar
- 59.Wang J, Shen J, Wu Y, Tu C, Soininen J, Stegen JC, He J, Liu X, Zhang L, Zhang E (2013) Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. ISME J 7:1310–1321. https://doi.org/10.1038/ismej.2013.30 CrossRefPubMedPubMedCentralGoogle Scholar
- 61.Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, PrincetonGoogle Scholar
- 67.Vega-Avila AD, Gumiere T, Andrade PAMM et al (2014) Bacterial communities in the rhizosphere of Vitis vinifera L. cultivated under distinct agricultural practices in Argentina. Antonie Van Leeuwenhoek, Int J Gen Mol Microbiol 107:575–588. https://doi.org/10.1007/s10482-014-0353-7 CrossRefPubMedGoogle Scholar