Ecological Processes Shaping Bulk Soil and Rhizosphere Microbiome Assembly in a Long-Term Amazon Forest-to-Agriculture Conversion

  • Dennis Goss-Souza
  • Lucas William MendesEmail author
  • Jorge Luiz Mazza Rodrigues
  • Siu Mui Tsai
Plant Microbe Interactions


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.


Metagenomics Microbial dispersal Neutral theory Selection Soybean rhizosphere 


Author Contributions

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.

Funding Information

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.

Supplementary material

248_2019_1401_MOESM1_ESM.pdf (1 mb)
ESM 1 (PDF 1074 kb)


  1. 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. Google Scholar
  2. 2.
    Navarrete AA, Kuramae EE, de Hollander M, Pijl AS, van Veen JA, Tsai SM (2013) Acidobacterial community responses to agricultural management of soybean in Amazon forest soils. FEMS Microbiol. Ecol. 83:607–621. Google Scholar
  3. 3.
    Communication S, Mueller RC, Paula FS et al (2014) Links between plant and fungal communities across a deforestation chronosequence in the Amazon rainforest. ISME J 8:1548–1550. Google Scholar
  4. 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. Google Scholar
  5. 5.
    Beisner BE, Haydon DT, Cuddington K (2003) Alternative stable states in ecology. Front. Ecol. Environ. 1:376–382Google Scholar
  6. 6.
    Mendes LW, Tsai SM, Navarrete AA, de Hollander M, van Veen JA, Kuramae EE (2015) Soil-borne microbiome: linking diversity to function. Microb. Ecol. 70:255–265. Google Scholar
  7. 7.
    Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8:1–11. Google Scholar
  8. 8.
    König S, Worrich A, Centler F, Wick LY, Miltner A, Kästner M, Thullner M, Frank K, Banitz T (2017) Modelling functional resilience of microbial ecosystems: analysis of governing processes. Environ. Model. Softw. 89:31–39. Google Scholar
  9. 9.
    Pérez-Jaramillo JE, Mendes R, Raaijmakers JM et al (2016) Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant Mol. Biol. 90:635–644. Google Scholar
  10. 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. Google Scholar
  11. 11.
    Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecol. Lett. 12:1238–1249. Google Scholar
  12. 12.
    Barberán A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6:343–351. Google Scholar
  13. 13.
    Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JBH (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol 10:497–506. Google Scholar
  14. 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. Google Scholar
  15. 15.
    Hovatter SR, Dejelo C, Case AL, Blackwood CB (2011) Metacommunity organization of soil microorganisms depends on habitat defined by presence of Lobelia siphilitica plants. Ecology 92:57–65Google Scholar
  16. 16.
    Jackson ND, Fahrig L (2014) Landscape context affects genetic diversity at a much larger spatial extent than population abundance. Ecology 95:871–881. Google Scholar
  17. 17.
    Rousk J, Baath E, Brookes PC et al (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351. Google Scholar
  18. 18.
    Dini-Andreote F, Stegen JC, van Elsas JD, Salles JF (2015) Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc. Natl. Acad. Sci. 201414261:E1326–E1332. Google Scholar
  19. 19.
    Pillar VD, Duarte LDS (2010) A framework for metacommunity analysis of phylogenetic structure. Ecol. Lett. 13:587–596. Google Scholar
  20. 20.
    Roughgarden J (2009) Is there a general theory of community ecology? Biol. Philos. 24:521–529. Google Scholar
  21. 21.
    Pholchan MK, Baptista J de C, Davenport RJ et al (2013) Microbial community assembly, theory and rare functions. Front. Microbiol. 4:1–9. Google Scholar
  22. 22.
    Colin Y, Nicolitch O, Van Nostrand JD et al (2017) Taxonomic and functional shifts in the beech rhizosphere microbiome across a natural soil toposequence. Sci. Rep. 7:1–17. Google Scholar
  23. 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. Google Scholar
  24. 24.
    Schlemper TR, Leite MFAA, Lucheta AR et al (2017) Rhizobacterial community structure differences among sorghum cultivars in different growth stages and soils. FEMS Microbiol. Ecol. 93:fix096. Google Scholar
  25. 25.
    Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, Rockhold ML, Konopka A (2013) Quantifying community assembly processes and identifying features that impose them. ISME J 7:2069–2079. Google Scholar
  26. 26.
    Dini-Andreote F, de Cássia Pereira E, Silva M, Triadó-Margarit X et al (2014) Dynamics of bacterial community succession in a salt marsh chronosequence: evidences for temporal niche partitioning. ISME J 8:1989–2001. Google Scholar
  27. 27.
    Goss-Souza D, Mendes LW, Borges CD et al (2017) Soil microbial community dynamics and assembly under long-term land use change. FEMS Microbiol. Ecol. 93:fix109. Google Scholar
  28. 28.
    Fitzpatrick CR, Copeland J, Wang PW, Guttman DS, Kotanen PM, Johnson MTJ (2018) Assembly and ecological function of the root microbiome across angiosperm plant species. Proc. Natl. Acad. Sci. 115:E1157–E1165. Google Scholar
  29. 29.
    Székely AJ, Langenheder S (2014) The importance of species sorting differs between habitat generalists and specialists in bacterial communities. FEMS Microbiol. Ecol. 87:102–112. Google Scholar
  30. 30.
    Cottenie K (2005) Integrating environmental and spatial processes in ecological community dynamics. Ecol. Lett. 8:1175–1182. Google Scholar
  31. 31.
    Ferrenberg S, O’Neill SP, Knelman JE et al (2013) Changes in assembly processes in soil bacterial communities following a wildfire disturbance. ISME J 7:1102–1111. Google Scholar
  32. 32.
    Powell JR, Karunaratne S, Campbell CD, Yao H, Robinson L, Singh BK (2015) Deterministic processes vary during community assembly for ecologically dissimilar taxa. Nat. Commun. 6:1–10. Google Scholar
  33. 33.
    Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2009) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:337–345. Google Scholar
  34. 34.
    Goss-Souza D, Mendes LW, Rodrigues JLM, Tsai SM (2019) Amazon forest-to-agriculture conversion alters rhizosphere microbiome composition while functions are kept. FEMS Microbiol. Ecol. 95:fiz009. Google Scholar
  35. 35.
    Gee GW, Bauder JW (1986) Particle-size analysis. In: Klute A (ed) Methods of soil analysis. ASA, Madison, pp 383–411Google Scholar
  36. 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. 37.
    Claessen MEC, Barreto WO, Paula JL, Duarte MN (1997) Manual of soil analysis methods2nd edn. Embrapa, Rio de JaneiroGoogle Scholar
  38. 38.
    Dhaliwal GS, Gupta N, Kukal SS, Kaur M (2011) Standardization of automated Vario EL III CHNS analyzer for total carbon and nitrogen determination in soils. Commun. Soil Sci. Plant Anal. 42:971–979. Google Scholar
  39. 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. 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
  41. 41.
    Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. Google Scholar
  42. 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
  43. 43.
    Wilke A, Bischof J, Gerlach W, Glass E, Harrison T, Keegan KP, Paczian T, Trimble WL, Bagchi S, Grama A, Chaterji S, Meyer F (2016) The MG-RAST metagenomics database and portal in 2015. Nucleic Acids Res. 44:D590–D594. Google Scholar
  44. 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. Google Scholar
  45. 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. Google Scholar
  46. 46.
    Paulson JN, Colin Stine O, Bravo HC, Pop M (2013) Differential abundance analysis for microbial marker-gene surveys. Nat. Methods 10:1200–1202. Google Scholar
  47. 47.
    Baselga A, Orme DL (2012) Betapart : an R package for the study of beta diversity. Methods Ecol. Evol. 3:808–812. Google Scholar
  48. 48.
    Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Glob. Ecol. Biogeogr. 19:134–143. Google Scholar
  49. 49.
    Jabot F, Etienne RS, Chave J (2008) Reconciling neutral community models and environmental filtering: theory and an empirical test. Oikos 117:1308–1320. Google Scholar
  50. 50.
    Feinstein LM, Blackwood CB (2012) Taxa-area relationship and neutral dynamics influence the diversity of fungal communities on senesced tree leaves. Environ. Microbiol. 14:1488–1499. Google Scholar
  51. 51.
    Bozdogan H (1987) Model selection and Akaike’s information criterion (AIC): the general theory and its analytical extensions. Psychometrika 52:345–370. Google Scholar
  52. 52.
    Etienne RS, Alonso D (2005) A dispersal-limited sampling theory for species and alleles. Ecol. Lett. 8:1147–1156. Google Scholar
  53. 53.
    Lepš J, Šmilauer P (2005) Multivariate analysis of ecological data using CANOCO. Bull. Ecol. Soc. Am. 86:6–6.[6a:MAOEDU]2.0.CO;2 Google Scholar
  54. 54.
    Fierer N (2017) Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol 15:579–590. Google Scholar
  55. 55.
    Vellend M (2010) Conceptual synthesis in community ecology. Q. Rev. Biol. 85:183–206Google Scholar
  56. 56.
    Hubbell SP (2005) Neutral theory in community ecology and the hypothesis of functional equivalence. Funct. Ecol. 19:166–172. Google Scholar
  57. 57.
    Tripathi BM, Stegen JC, Kim M, Dong K, Adams JM, Lee YK (2018) Soil pH mediates the balance between stochastic and deterministic assembly of bacteria. ISME J 12:1072–1083. Google Scholar
  58. 58.
    Stegen JC, Lin X, Fredrickson JK, Konopka AE (2015) Estimating and mapping ecological processes influencing microbial community assembly. Front. Microbiol. 6:1–15. Google Scholar
  59. 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. Google Scholar
  60. 60.
    Kielak AM, Scheublin TR, Mendes LW, van Veen JA, Kuramae EE (2016) Bacterial community succession in pine-wood decomposition. Front. Microbiol. 7:1–12. Google Scholar
  61. 61.
    Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, PrincetonGoogle Scholar
  62. 62.
    Mutshinda CM, O’Hara RB (2011) Integrating the niche and neutral perspectives on community structure and dynamics. Oecologia 166:241–251Google Scholar
  63. 63.
    Fukami T, Nakajima M (2011) Community assembly: alternative stable states or alternative transient states? Ecol. Lett. 14:973–984. Google Scholar
  64. 64.
    Maaß S, Migliorini M, Rillig MC, Caruso T (2014) Disturbance, neutral theory, and patterns of beta diversity in soil communities. Ecol Evol 4:4766–4774. Google Scholar
  65. 65.
    McGill BJ, Maurer BA, Weiser MD (2006) Empirical evaluation of neutral theory. Ecology 87:1411–1423Google Scholar
  66. 66.
    Jia X, Dini-Andreote F, Falcão Salles J (2018) Community assembly processes of the microbial rare biosphere. Trends Microbiol. 26:738–747. Google Scholar
  67. 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. Google Scholar
  68. 68.
    Qiao Q, Wang F, Zhang JJ, Chen Y, Zhang C, Liu G, Zhang H, Ma C, Zhang J (2017) The variation in the rhizosphere microbiome of cotton with soil type, genotype and developmental stage. Sci. Rep. 7(3940):3940. Google Scholar
  69. 69.
    Nacke H, Fischer C, Thürmer A, Meinicke P, Daniel R (2014) Land use type significantly affects microbial gene transcription in soil. Microb. Ecol. 67:919–930. Google Scholar
  70. 70.
    Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. U. S. A. 103:626–631Google Scholar
  71. 71.
    Attard E, Recous S, Chabbi a et al (2011) Soil environmental conditions rather than denitrifier abundance and diversity drive potential denitrification after changes in land uses. Glob. Chang. Biol. 17:1975–1989. Google Scholar
  72. 72.
    Drenovsky RE, Steenwerth KL, Jackson LE, Scow KM (2010) Land use and climatic factors structure regional patterns in soil microbial communities. Glob. Ecol. Biogeogr. 19:27–39. Google Scholar
  73. 73.
    Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microbiol. 75:5111–5120. Google Scholar
  74. 74.
    Tucker CM, Fukami T (2014) Environmental variability counteracts priority effects to facilitate species coexistence : evidence from nectar microbes. Proc. R. Soc. B 281:1–9. Google Scholar
  75. 75.
    Shade A, Peter H, Allison SD et al (2012) Fundamentals of microbial community resistance and resilience. Front. Microbiol. 3:1–19. Google Scholar
  76. 76.
    Sugiyama A, Ueda Y, Zushi T, Takase H, Yazaki K (2014) Changes in the bacterial community of soybean rhizospheres during growth in the field. PLoS One 9:e100709. Google Scholar

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Authors and Affiliations

  1. 1.Center for Nuclear Energy in AgricultureUniversity of São PauloPiracicabaBrazil
  2. 2.Department of Land, Air and Water ResourcesUniversity of California – DavisDavisUSA
  3. 3.Department of Soils and Natural ResourcesSanta Catarina State UniversityLagesBrazil
  4. 4.Environmental Genomics and Systems Biology DivisionLawrence Berkeley National LaboratoryBerkeleyUSA

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