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The role of species turnover in structuring bacterial communities in a local scale in the cactus rhizosphere

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Abstract

Background and aims

Cereus jamacaru is a native cactus in the semiarid biome caatinga able to withstand long periods of drought. Here, we studied the rhizosphere microbiome of this cactus to understand how precipitation affects the assembly of bacterial communities from the taxonomical and functional perspectives.

Methods

We selected three C. jamacaru plants in the caatinga biome, sampled the rhizosphere soil from the same plants during rainy and dry seasons and performed shotgun sequencing from total DNA isolated from rhizosphere using Ion Torrent technology.

Results

Acidobacteria, Actinobacteria and Proteobacteria showed increase in relative abundance during the rainy season when compared to dry season. Five major functional groups were significantly different, including differences in amino acids and derivatives, carbohydrates, protein metabolism, respiration, and RNA metabolism. Taxonomically, the assembly of bacterial communities follows a neutral model.

Conclusions

The assembly of bacterial communities in the rhizosphere of C. jamacaru is affected by precipitation resulting in different taxonomical and functional community patterns during dry and rainy seasons. We attribute these differences on rhizosphere communities composition to dispersal limitation of microorganisms caused by low pore connectivity due to low water content in the soil, which leads to spatially isolate communities during the dry season.

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References

  • Adams RI, Miletto M, Taylor JW, Bruns TD (2013) Dispersal in microbes: fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances. ISME J 7(7):1262–1273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Caski F (eds) Proceedings of the second international symposium on information theory. Akademiai Kiado, Budapest, pp 267–281

    Google Scholar 

  • Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Glob Ecol Biogeogr 19:134–143

    Article  Google Scholar 

  • Baselga A, Orme CDL (2012) Betapart: an R package for the study of beta diversity. Methods Ecol Evol 3:808–812

    Article  Google Scholar 

  • Bilton DT, Freeland JR, Okamura B (2001) Dispersal in freshwater invertebrates. Annu Rev Ecol Syst 32:159–181

    Article  Google Scholar 

  • Blankenberg D, Gordon A, Von Kuster G, Coraor N, Taylor J, Nekrutenko A, Galaxy Team (2010) Manipulation of FASTQ data with galaxy. Bioinformatics 26(14):1783–1785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carson JK, Gonzalez-Quiñones V, Murphy DV, Hinz C, Shaw JA, Gleeson DB (2010) Low pore connectivity increases bacterial diversity in soil. Appl Environ Microbiol 76(12):3936–3942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW (2010) Soil microbial community responses to multiple experimental climate change drivers. Appl Environ Microbiol 76(4):999–1007

    Article  CAS  PubMed  Google Scholar 

  • Chan Y, Van Nostrand JD, Zhou J, Pointing SB, Farrell RL (2013) Functional ecology of an Antarctic Dry Valley. Proc Natl Acad Sci U S A 110(22):8990–8995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chase JM (2007) Drought mediates the importance of stochastic community assembly. Proc Natl Acad Sci U S A 104:17430–17434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen LZ, Li DH, Song LR, Hu CX, Wang GH, Liu YD (2006) Effects of salt stress on carbohydrate metabolism in desert soil alga Microcoleus vaginatus Gom. J Integr Plant Biol 48(8):914–919

    Article  CAS  Google Scholar 

  • De Mesel I, Derycke S, Moens T, Van der Gucht K, Vincx M, Swings J (2004) Top-down impact of bacterivorous nematodes on the bacterial community structure: a microcosm study. Environ Microbiol 6(7):733–744

    Article  PubMed  Google Scholar 

  • Dechesne A, Or D, Smets BF (2008) Limited diffusive fluxes of substrate facilitate coexistence of two competing bacterial strains. FEMS Microbiol Ecol 64:1–8

    Article  CAS  PubMed  Google Scholar 

  • Dechesne A, Wang G, Gülez G, Or D, Smetsa BF (2010) Hydration-controlled bacterial motility and dispersal on surfaces. Proc Natl Acad Sci U S A 107(32):14369–14372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diallo MD, Willems A, Vloemans N, Cousin S, Vandekerckhove TT, de Lajudie P, Neyra M, Vyverman W, Gillis M, Van der Gucht K (2004) Polymerase chain reaction denaturing gradient gel electrophoresis analysis of the N2-fixing bacterial diversity in soil under Acacia tortilis ssp. raddiana and Balanites aegyptiaca in the dryland part of Senegal. Environ Microbiol 6(4):400–415

    Article  CAS  Google Scholar 

  • Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, Brulc JM, Furlan M, Desnues C, Haynes M, Li L, McDaniel L, Moran MA, Nelson KE, Nilsson C, Olson R, Paul J, Brito BR, Ruan Y, Swan BK, Stevens R, Valentine DL, Thurber RV, Wegley L, White BA, Rohwer F (2008) Functional metagenomic profiling of nine biomes. Nature 452(7187):629–632

    Article  CAS  PubMed  Google Scholar 

  • Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4(3):337–345

    Article  PubMed  Google Scholar 

  • Eichorst SA, Breznak JA, Schmidt TM (2007) Isolation and characterization of soil bacteria that define Terriglobus gen. nov., in the phylum Acidobacteria. Appl Environ Microbiol 73(8):2708–2717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eisenlord SD, Zak DR, Upchurch RA (2012) Dispersal limitation and the assembly of soil Actinobacteria communities in a long-term chronosequence. Ecol Evol 2(3):538–549

    Article  PubMed  PubMed Central  Google Scholar 

  • Etienne RS, Olff H (2005) Confronting different models of community structure to species-abundance data: a Bayesian model comparison. Ecol Lett 8(5):493–504

    Article  PubMed  Google Scholar 

  • Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6(5):1007–1017

    Article  CAS  PubMed  Google Scholar 

  • Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296(5570):1061–1063

    Article  CAS  PubMed  Google Scholar 

  • Giulietti AM, Harley R, Queiroz LP, Rapini A (2006) To set the scene. In: Queiroz LP, Rapini A, Giulietti AM (eds) Towards greater knowledge of the Brazilian semi-arid biodiversity. Brasília, Ministério de Ciência e Tecnologia, pp 11–15

    Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) Past: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1) art. 4

  • Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Monographs in population biology (MPB-32). Princeton University Press, Princeton

    Google Scholar 

  • Jabot F, Etienne RS, Chave J (2008) Reconciling neutral community models and environmental filtering: theory and an empirical test. Oikos 117(9):1308–1320

  • Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3(4):442–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kakumanu ML, Cantrell CL, Williams MA (2013) Microbial community response to varying magnitudes of desiccation in soil: a test of the osmolyte accumulation hypothesis. Soil Biol Biochem 57:644–653

    Article  CAS  Google Scholar 

  • Kavamura VN, Taketani RG, Lançoni MD, Andreote FD, Mendes R, Soares de Melo I (2013) Water regime influences bulk soil and rhizosphere of Cereus jamacaru bacterial communities in the Brazilian Caatinga biome. PLoS One 8(9):e73606

    Article  CAS  Google Scholar 

  • Kröber M, Wibberg D, Grosch R, Eikmeyer F, Verwaaijen B, Chowdhury SP, Hartmann A, Pühler A, Schlüter A (2014) Effect of the strain Bacillus amyloliquefaciens FZB42 on the microbial community in the rhizosphere of lettuce under field conditions analyzed by whole metagenome sequencing. Front Microbiol 5:252

    PubMed  PubMed Central  Google Scholar 

  • Lançoni MD, Taketani RG, Kavamura VN, de Melo IS (2013) Microbial community biogeographic patterns in the rhizosphere of two Brazilian semi-arid leguminous trees. World J Microbiol Biotechnol 29(7):1233–1241

    Article  PubMed  Google Scholar 

  • Leibold MA, McPeek MA (2006) Coexistence of the niche and neutral perspectives in community ecology. Ecology 87(6):1399–1410

    Article  PubMed  Google Scholar 

  • Lindström ES, Langenheder S (2012) Local and regional factors influencing bacterial community assembly. Environ Microbiol Rep 4(1):1–9

    Article  PubMed  Google Scholar 

  • Lopes PM, Bini LM, Declerck SAJ, Farjalla VF, Vieira LCG, Bonecker CC, Lansac-Toha FA, Esteves FA, Bozelli RL (2014) Correlates of zooplankton beta diversity in tropical lake systems. PLoS ONE 9(10):e109581

  • Manzoni S, Taylor P, Richter A, Porporato A, Agren GI (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196(1):79–91

    Article  CAS  PubMed  Google Scholar 

  • McGill BJ, Etienne RS, Gray JS, Alonso D, Anderson MJ, Benecha HK, Dornelas M, Enquist BJ, Green JL, He F, Hurlbert AH, Magurran AE, Marquet PA, Maurer BA, Ostling A, Soykan CU, Ugland KI, White EP (2007) Species abundance distributions: moving beyond single prediction theories to integration within an ecological framework. Ecol Lett 10(10):995–1015

    Article  PubMed  Google Scholar 

  • McKew BA, Taylor JD, McGenity TJ, Underwood GJ (2011) Resistance and resilience of benthic biofilm communities from a temperate saltmarsh to desiccation and rewetting. ISME J 5(1):30–41

    Article  PubMed  Google Scholar 

  • McNeil SD, Nuccio ML, Hanson AD (1999) Betaines and related osmoprotectants. Targets for metabolic engineering of stress resistance. Plant Physiol 120(4):945–950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8(8):1577–1587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menezes RS, Sampaio EV, Giongo V, Pérez-Marin AM (2012) Biogeochemical cycling in terrestrial ecosystems of the Caatinga biome. Braz J Biol 72(3):643–653

    Article  CAS  PubMed  Google Scholar 

  • Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA (2008) The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinf 9:386

    Article  CAS  Google Scholar 

  • Motomura I (1932) A statistical treatment of associations [in Japanese]. Jap J Zool 44:379–383

    Google Scholar 

  • Nocker A, Fernández PS, Montijn R, Schuren F (2012) Effect of air drying on bacterial viability: a multiparameter viability assessment. J Microbiol Methods 90(2):86–95

    Article  CAS  PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL, Solymos P, Stevens HH, Wagner H (2010) Vegan: community ecology package. R package version 1.17–1

  • Pacchioni RG, Carvalho FM, Thompson CE, Faustino AL, Nicolini F, Pereira TS, Silva RC, Cantão ME, Gerber A, Vasconcelos AT, Agnez-Lima LF (2014) Taxonomic and functional profiles of soil samples from Atlantic forest and Caatinga biomes in northeastern Brazil. Microbiology 3(3):299–315

    CAS  Google Scholar 

  • Peay KG, Schubert MG, Nguyen NH, Bruns TD (2012) Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol 21(16):4122–4136

    Article  PubMed  Google Scholar 

  • Placella SA, Brodie EL, Firestone MK (2012) Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups. Proc Natl Acad Sci U S A 109(27):10931–10936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian H, Ricklefs RE, White PS (2005) Beta diversity of angiosperms in temperate floras of eastern Asia and eastern North America. Ecol Lett 8:15–22

    Article  Google Scholar 

  • Rádková V, Bojková J, Křoupalová V, Schenková J, Syrovátka V, Horsák M (2014) The role of dispersal mode and habitat specialisation in metacommunity structuring of aquatic macroinvertebrates in isolated spring fens. Freshw Biol 59:2256–2267

    Article  Google Scholar 

  • Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88(6):1386–1394

    Article  PubMed  Google Scholar 

  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6):R60

    Article  PubMed  PubMed Central  Google Scholar 

  • Song F, Han X, Zhu X, Herbert SJ (2012) Response to water stress of soil enzymes and root exudates from drought and non-drought tolerant corn hybrids at different growth stages. Can J Soil Sci 92(3):501–507

    Article  CAS  Google Scholar 

  • Stark JM, Firestone MK (1995) Mechanisms for soil moisture effects on activity of nitrifying bacteria. Appl Environ Microbiol 61:218–221

    CAS  PubMed  PubMed Central  Google Scholar 

  • Taketani RG, Kavamura VN, Mendes R, Melo IS (2015) Functional congruence of rhizosphere microbial communities associated to leguminous tree from Brazilian semiarid region. Environ Microbiol Rep 7(1):95–101

    Article  CAS  PubMed  Google Scholar 

  • Taketani RG, Lançoni MD, Kavamura VN, Durrer A, Andreote FD, Melo IS (2017) Dry season constrains bacterial phylogenetic diversity in a semi-arid rhizosphere system. Microb Ecol 73:153–161

    Article  PubMed  Google Scholar 

  • Thompson R, Townsend C (2006) A truce with neutral theory: local deterministic factors, species traits and dispersal limitation together determine patterns of diversity in stream invertebrates. J Anim Ecol 75(2):476–484

    Article  PubMed  Google Scholar 

  • Torres-Cortés G, Millán V, Fernández-González AJ, Aguirre-Garrido JF, Ramírez-Saad HC, Toro N, Martínesz-Abarca F (2012) Bacterial community in the rhizosphere of the cactus species Mammillaria carnea during dry and rainy seasons assessed by deep sequencing. Plant Soil 357:275–288

    Article  Google Scholar 

  • Treves DS, Xia B, Zhou J, Tiedje JM (2003) A two-species test of the hypothesis that spatial isolation influences microbial diversity in soil. Microb Ecol 45:20–28

    Article  CAS  PubMed  Google Scholar 

  • Ude S, Arnold DL, Moon CD, Timms-Wilson T, Spiers AJ (2006) Biofilm formation and cellulose expression among diverse environmental Pseudomonas isolates. Environ Microbiol 8(11):1997–2011

    Article  CAS  PubMed  Google Scholar 

  • van der Walt AJ, van Goethem MW, Ramond JB, Makhalanyane TP, Reva O, Cowan DA (2017) Assembling metagenomes, one community at a time. BMC Genomics 18:521

    Article  PubMed  PubMed Central  Google Scholar 

  • Vos M, Velicer GJ (2008) Natural variation of gliding motility in a centimetre-scale population of Myxococcus xanthus. FEMS Microbiol Ecol 64(3):343–350

    Article  CAS  PubMed  Google Scholar 

  • Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132(1):44–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M, Badger J, Barabote RD, Bradley B, Brettin TS, Brinkac LM, Bruce D, Creasy T, Daugherty SC, Davidsen TM, DeBoy RT, Detter JC, Dodson RJ, Durkin AS, Ganapathy A, Gwinn-Giglio M, Han CS, Khouri H, Kiss H, Kothari SP, Madupu R, Nelson KE, Nelson WC, Paulsen I, Penn K, Ren Q, Rosovitz MJ, Selengut JD, Shrivastava S, Sullivan SA, Tapia R, Thompson LS, Watkins KL, Yang Q, Yu C, Zafar N, Zhou L, Kuske CR (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75(7):2046–2056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whitaker RJ, Grogan DW, Taylor JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301(5635):976–978

    Article  CAS  PubMed  Google Scholar 

  • Wolf AB, Vos M, de Boer W, Kowalchuk GA (2013) Impact of matric potential and pore size distribution on growth dynamics of filamentous and non-filamentous soil bacteria. PLoS One 8(12):e83661

    Article  PubMed  PubMed Central  Google Scholar 

  • Wood JM, Bremer E, Csonka LN, Kraemer R, Poolman B, van der Heide T, Smith LT (2001) Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp Biochem Physiol A Mol Integr Physiol 130(3):437–460

    Article  CAS  PubMed  Google Scholar 

  • Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208(15):2819–3280

    Article  CAS  PubMed  Google Scholar 

  • Yuste JC, Fernandez-Gonzalez AJ, Fernandez-Lopez M, Ogaya R, Penuelas J, Lloret F (2014) Functional diversification within bacterial lineages promotes wide functional overlapping between taxonomic groups in a Mediterranean forest soil. FEMS Microbiol Ecol 90(1):54–67

    Article  Google Scholar 

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Acknowledgments

This work was funded by Embrapa grant SEG 02.09.01.008.00.00. We thank FAPESP for scholarship support provided to V. N. K. (2013/08144-1, 2014/16041-0), R. G. T. (2010/50799-7, 2013/23470-2) and C. F. (2011/15760-5). The authors also thank João Luiz da Silva and Carlos Alberto Tuão Gava for their help on sampling expeditions in the Caatinga biome and Dr. Ademir Durrer for performing the TAD fitting models. We thank S. R. Cotta for critical reading and valuable suggestions.

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Authors and Affiliations

  1. Embrapa Meio Ambiente, Rodovia SP-340 km 127,5, Jaguariúna, SP, Brazil

    Vanessa Nessner Kavamura, Rodrigo Gouvêa Taketani, Clederson Ferreira, Itamar Soares de Melo & Rodrigo Mendes

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  1. Vanessa Nessner Kavamura
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  2. Rodrigo Gouvêa Taketani
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  3. Clederson Ferreira
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  4. Itamar Soares de Melo
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  5. Rodrigo Mendes
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Correspondence to Rodrigo Mendes.

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Kavamura, V.N., Taketani, R.G., Ferreira, C. et al. The role of species turnover in structuring bacterial communities in a local scale in the cactus rhizosphere. Plant Soil 425, 101–112 (2018). https://doi.org/10.1007/s11104-018-3570-4

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