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Moisture Is More Important than Temperature for Assembly of Both Potentially Active and Whole Prokaryotic Communities in Subtropical Grassland

  • Soil Microbiology
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Abstract

Moisture and temperature play important roles in the assembly and functioning of prokaryotic communities in soil. However, how moisture and temperature regulate the function of niche- versus neutral-based processes during the assembly of these communities has not been examined considering both the total microbial community and the sole active portion with potential for growth in native subtropical grassland. We set up a well-controlled microcosm-based experiment to investigate the individual and combined effects of moisture and temperature on soil prokaryotic communities by simulating subtropical seasons in grassland. The prokaryotic populations with potential for growth and the total prokaryotic community were assessed by 16S rRNA transcript and 16S rRNA gene analyses, respectively. Moisture was the major factor influencing community diversity and structure, with a considerable effect of this factor on the total community. The prokaryotic populations with potential for growth and the total communities were influenced by the same assembly rules, with the niche-based mechanism being more influential in communities under dry condition. Our results provide new information regarding moisture and temperature in microbial communities of soil and elucidate how coexisting prokaryotic populations, under different physiological statuses, are shaped in native subtropical grassland soil.

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Data Accessibility

All raw sequences were deposited in the Sequence Read Archive (SRA) under the study accession number PRJEB10903 (http://www.ebi.ac.uk/ena/data/view/PRJEB10903).

References

  1. Deng Q, Hui D, Zhang D, Zhou G, Liu J, Liu S, Chu G, Li J (2012) Effects of precipitation increase on soil respiration: a three-year field experiment in subtropical forests in China. PLoS One 7:e41493. https://doi.org/10.1371/journal.pone.0041493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. 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 

  3. Karhu K, Auffret MD, Dungait JAJ, Hopkins DW, Prosser JI, Singh BK, Subke JA, Wookey PA, Ågren GI, Sebastià MT, Gouriveau F, Bergkvist G, Meir P, Nottingham AT, Salinas N, Hartley IP (2014) Temperature sensitivity of soil respiration rates enhanced by microbial community response. Nature 513:81–84

    Article  CAS  PubMed  Google Scholar 

  4. Lipson DA (2007) Relationships between temperature responses and bacterial community structure along seasonal and altitudinal gradients. FEMS Microbiol Ecol 59:418–427. https://doi.org/10.1111/j.1574-6941.2006.00240.x

    Article  CAS  PubMed  Google Scholar 

  5. Chemidlin Prevost-Boure N, Maron P-A, Ranjard L, Nowak V, Dufrene E, Damesin C, Soudani K, Lata JC (2011) Seasonal dynamics of the bacterial community in forest soils under different quantities of leaf litter. Appl Soil Ecol 47:14–23. https://doi.org/10.1016/j.apsoil.2010.11.006

    Article  Google Scholar 

  6. Young IM (2004) Interactions and self-organization in the soil-microbe complex. Science 304:1634–1637. https://doi.org/10.1126/science.1097394

    Article  CAS  PubMed  Google Scholar 

  7. Bell C, McIntyre N, Cox S, Tissue D, Zak J (2008) Soil microbial responses to temporal variations of moisture and temperature in a Chihuahuan Desert Grassland. Microb Ecol 56:153–167. https://doi.org/10.1007/s00248-007-9333-z

    Article  PubMed  Google Scholar 

  8. Brockett BFT, Prescott CE, Grayston SJ (2012) Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol Biochem 44:9–20. https://doi.org/10.1016/j.soilbio.2011.09.003

    Article  CAS  Google Scholar 

  9. Stres B, Danevčič T, Pal L et al (2008) Influence of temperature and soil water content on bacterial, archaeal and denitrifying microbial communities in drained fen grassland soil microcosms. FEMS Microbiol Ecol 66:110–122. https://doi.org/10.1111/j.1574-6941.2008.00555.x

    Article  CAS  PubMed  Google Scholar 

  10. Kennedy NM, Gleeson DE, Connolly J, Clipson NJW (2005) Seasonal and management influences on bacterial community structure in an upland grassland soil. FEMS Microbiol Ecol 53:329–337. https://doi.org/10.1016/j.femsec.2005.01.013

    Article  CAS  PubMed  Google Scholar 

  11. Williams MA, Jangid K, Shanmugam SG, Whitman WB (2013) Bacterial communities in soil mimic patterns of vegetative succession and ecosystem climax but are resilient to change between seasons. Soil Biol Biochem 57:749–757. https://doi.org/10.1016/j.soilbio.2012.08.023

    Article  CAS  Google Scholar 

  12. Wang X, Wang X, Zhang W, Shao Y, Zou X, Liu T, Zhou L, Wan S, Rao X, Li Z, Fu S (2016) Invariant community structure of soil bacteria in subtropical coniferous and broadleaved forests. Sci Rep 6(19071). https://doi.org/10.1038/srep19071

  13. Smit E, Leeflang P, Gommans S, van den Broek J, van Mil S, Wernars K (2001) Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl Environ Microbiol 67:2284–2291. https://doi.org/10.1128/AEM.67.5.2284-2291.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. 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. https://doi.org/10.1038/ismej.2013.11

    Article  PubMed  PubMed Central  Google Scholar 

  15. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  17. Valverde A, Makhalanyane TP, Cowan DA (2014) Contrasting assembly processes in a bacterial metacommunity along a desiccation gradient. Front Microbiol 5. https://doi.org/10.3389/fmicb.2014.00668

  18. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505

    Article  Google Scholar 

  19. Horner-Devine MC, Bohannan BJM (2006) Phylogenetic clustering and overdispersion in bacterial communities. Ecology 87:S100–S108. https://doi.org/10.1890/0012-9658(2006)87[100:PCAOIB]2.0.CO;2

  20. Jones CM, Hallin S (2010) Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME J 4:633–641

    Article  PubMed  Google Scholar 

  21. Stegen JC, Lin X, Konopka AE, Fredrickson JK (2012) Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J 6:1653–1664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Barboza ADM, Pylro VS, Jacques RJS, Gubiani PI, de Quadros FLF, Trindade JK, Triplett EW, Roesch L (2018) Seasonal dynamics alter taxonomical and functional microbial profiles in Pampa biome soils under natural grasslands. PeerJ 6:e4991. https://doi.org/10.7717/peerj.4991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Roesch LFW, Vieira FCB, Pereira VA et al (2009) The Brazilian Pampa: a fragile biome. Diversity 1:182–198

    Article  Google Scholar 

  24. Overbeck GE, Müller SC, Fidelis A et al (2007) Brazil’s neglected biome: the South Brazilian Campos. Perspect Plant Ecol Evol Syst 9:101–116. https://doi.org/10.1016/j.ppees.2007.07.005

    Article  Google Scholar 

  25. Klute A (1986) Methods of soil analysis: part 1—physical and mineralogical methods. Soil Science Society of America, American Society of Agronomy, Madison

    Google Scholar 

  26. Reinert DJ, Reichert JM (2006) Coluna de areia para medir a retenção de água no solo: protótipos e teste. Ciênc Rural 36:1931–1935

    Article  Google Scholar 

  27. da Silva FC (Ed.) (2009) Manual de análises químicas de solos, plantas e fertilizantes. Embrapa Informação Tecnológica; Rio de Janeiro: Embrapa Solos, Brasília

  28. Ritz K, McNicol JW, Nunan N et al (2004) Spatial structure in soil chemical and microbiological properties in an upland grassland. FEMS Microbiol Ecol 49:191–205. https://doi.org/10.1016/j.femsec.2004.03.005

    Article  CAS  PubMed  Google Scholar 

  29. Conte O, de Wesp CL, Anghinoni I, et al (2011) Densidade, agregação e frações de carbono de um argissolo sob pastagem natural submetida a níveis de ofertas de forragem por longo tempo. Rev Bras Ciênc Solo Camp 35(2): 579–587. Marabr 2011

  30. 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 

  31. Dobbler PT, Procianoy RS, Mai V, Silveira RC, Corso AL, Rojas BS, Roesch LFW (2017) Low microbial diversity and abnormal microbial succession is associated with necrotizing enterocolitis in preterm infants. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.02243

  32. Pylro VS, Roesch LFW, Morais DK, Clark IM, Hirsch PR, Tótola MR (2014) Data analysis for 16S microbial profiling from different benchtop sequencing platforms. J Microbiol Methods 107:30–37. https://doi.org/10.1016/j.mimet.2014.08.018

    Article  CAS  PubMed  Google Scholar 

  33. Pylro VS, Morais DK, de Oliveira FS, dos Santos FG, Lemos LN, Oliveira G, Roesch LFW (2016) BMPOS: a flexible and user-friendly tool sets for microbiome studies. Microb Ecol 72:443–447

    Article  PubMed  Google Scholar 

  34. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604

    Article  CAS  PubMed  Google Scholar 

  35. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Claesson MJ, O’Sullivan O, Wang Q et al (2009) Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS One 4:e6669. https://doi.org/10.1371/journal.pone.0006669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Sheneman L, Evans J, Foster JA (2006) Clearcut: a fast implementation of relaxed neighbor joining. Bioinformatics 22:2823–2824. https://doi.org/10.1093/bioinformatics/btl478

    Article  CAS  PubMed  Google Scholar 

  39. R Development Core Team (2008) R: a language and environment for statistical computing

  40. McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. https://doi.org/10.1371/journal.pone.0061217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264

    Article  Google Scholar 

  42. Lemos et al (2011) Rethinking microbial diversity analysis in the hig.pdf

  43. Anderson MJ (2017) Permutational multivariate analysis of variance (PERMANOVA). In: Balakrishnan N, Colton T, Everitt B et al (eds) Wiley StatsRef: Statistics Reference Online. Wiley, Chichester, pp 1–15

    Google Scholar 

  44. Oksanen J, Blanchet F G, Kindt R, et al (2015) Vegan: community ecology package. R package vegan, vers. 2.2–1

  45. Kembel SW, Hubbell SP (2006) The phylogenetic structure of a neotropical forest tree community. Ecology 87:S86–S99. https://doi.org/10.1890/0012-9658(2006)87[86:TPSOAN]2.0.CO;2

  46. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15. https://doi.org/10.1186/s13059-014-0550-8

  47. Van der Putten WH (2012) Climate change, aboveground-belowground interactions, and species’ range shifts. Annu Rev Ecol Evol Syst 43:365–383. https://doi.org/10.1146/annurev-ecolsys-110411-160423

    Article  Google Scholar 

  48. Ellis RJ (2004) Artificial soil microcosms: a tool for studying microbial autecology under controlled conditions. J Microbiol Methods 56:287–290. https://doi.org/10.1016/j.mimet.2003.10.005

    Article  PubMed  Google Scholar 

  49. Jessup CM, Kassen R, Forde SE et al (2004) Big questions, small worlds: microbial model systems in ecology. Trends Ecol Evol 19:189–197. https://doi.org/10.1016/j.tree.2004.01.008

    Article  PubMed  Google Scholar 

  50. Srivastava DS, Kolasa J (2004) Bengtsson J, et al are natural microcosms useful model systems for ecology? Trends Ecol Evol 19:379–384. https://doi.org/10.1016/j.tree.2004.04.010

    Article  PubMed  Google Scholar 

  51. Eller G, Krüger M, Frenzel P (2005) Comparing field and microcosm experiments: a case study on methano- and methylo-trophic bacteria in paddy soil. FEMS Microbiol Ecol 51:279–291. https://doi.org/10.1016/j.femsec.2004.09.007

    Article  CAS  PubMed  Google Scholar 

  52. Baveye PC, Berthelin J, Munch J-C (2016) Too much or not enough: reflection on two contrasting perspectives on soil biodiversity. Soil Biol Biochem 103:320–326. https://doi.org/10.1016/j.soilbio.2016.09.008

    Article  CAS  Google Scholar 

  53. Bouskill NJ, Lim HC, Borglin S, Salve R, Wood TE, Silver WL, Brodie EL (2013) Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought. ISME J 7:384–394. https://doi.org/10.1038/ismej.2012.113

    Article  CAS  PubMed  Google Scholar 

  54. Cruz-Martínez K, Suttle KB, Brodie EL, Power ME, Andersen GL, Banfield JF (2009) Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland. ISME J 3:738–744

    Article  CAS  PubMed  Google Scholar 

  55. Barnard RL, Osborne CA, Firestone MK (2015) Changing precipitation pattern alters soil microbial community response to wet-up under a Mediterranean-type climate. ISME J 9:946–957

    Article  CAS  PubMed  Google Scholar 

  56. Chase JM, Myers JA (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Philos Trans R Soc B Biol Sci 366:2351–2363. https://doi.org/10.1098/rstb.2011.0063

    Article  Google Scholar 

  57. Ding J, Zhang Y, Deng Y, Cong J, Lu H, Sun X, Yang C, Yuan T, van Nostrand JD, Li D, Zhou J, Yang Y (2015) Integrated metagenomics and network analysis of soil microbial community of the forest timberline. Sci Rep 5. https://doi.org/10.1038/srep07994

  58. Jangid K, Williams MA, Franzluebbers AJ, Schmidt TM, Coleman DC, Whitman WB (2011) Land-use history has a stronger impact on soil microbial community composition than aboveground vegetation and soil properties. Soil Biol Biochem 43:2184–2193. https://doi.org/10.1016/j.soilbio.2011.06.022

    Article  CAS  Google Scholar 

  59. Hahn MW, Pockl M (2005) Ecotypes of planktonic Actinobacteria with identical 16S rRNA genes adapted to thermal niches in temperate, subtropical, and tropical freshwater habitats. Appl Environ Microbiol 71:766–773. https://doi.org/10.1128/AEM.71.2.766-773.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Schindlbacher A, Rodler A, Kuffner M, Kitzler B, Sessitsch A, Zechmeister-Boltenstern S (2011) Experimental warming effects on the microbial community of a temperate mountain forest soil. Soil Biol Biochem 43:1417–1425. https://doi.org/10.1016/j.soilbio.2011.03.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Wallenstein MD, Hall EK (2012) A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning. Biogeochemistry 109:35–47. https://doi.org/10.1007/s10533-011-9641-8

    Article  Google Scholar 

  62. Zhou W, Hui D, Shen W (2014) Effects of soil moisture on the temperature sensitivity of soil heterotrophic respiration: a laboratory incubation study. PLoS One 9:e92531. https://doi.org/10.1371/journal.pone.0092531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Strunk T, Currie A, Richmond P, Simmer K, Burgner D (2011) Innate immunity in human newborn infants: prematurity means more than immaturity. J Matern Fetal Neonatal Med 24:25–31. https://doi.org/10.3109/14767058.2010.482605

    Article  PubMed  Google Scholar 

  64. French S, Levy-Booth D, Samarajeewa A, Shannon KE, Smith J, Trevors JT (2009) Elevated temperatures and carbon dioxide concentrations: effects on selected microbial activities in temperate agricultural soils. World J Microbiol Biotechnol 25:1887–1900. https://doi.org/10.1007/s11274-009-0107-2

    Article  CAS  Google Scholar 

  65. Zhou J, Xia B, Treves DS, Wu LY, Marsh TL, O'Neill RV, Palumbo AV, Tiedje JM (2002) Spatial and resource factors influencing high microbial diversity in soil. Appl Environ Microbiol 68:326–334. https://doi.org/10.1128/AEM.68.1.326-334.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. 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. https://doi.org/10.1007/s00248-002-1044-x

    Article  CAS  PubMed  Google Scholar 

  67. Evans SE, Wallenstein MD (2014) Climate change alters ecological strategies of soil bacteria. Ecol Lett 17:155–164. https://doi.org/10.1111/ele.12206

    Article  PubMed  Google Scholar 

  68. 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

    Article  PubMed  PubMed Central  Google Scholar 

  69. 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 4:337–345

    Article  PubMed  Google Scholar 

  70. Rigg JL, Offord CA, Singh BK, Anderson IC, Clarke S, Powell JR (2016) Variation in soil microbial communities associated with critically endangered Wollemi pine affects fungal, but not bacterial, assembly within seedling roots. Pedobiologia 59:61–71. https://doi.org/10.1016/j.pedobi.2016.02.002

    Article  Google Scholar 

  71. Pholchan MK, Baptista J de C, Davenport RJ et al (2013) Microbial community assembly, theory and rare functions. Front Microbiol 4. https://doi.org/10.3389/fmicb.2013.00068

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Acknowledgements

The authors acknowledge M. Dresher for the assistance in the setup of the microcosm experiment, P. Gubiani for soil physical discussions and assistance in the field to measure moisture and temperature over the year, and Z.I. Antoniolli for laboratory structure.

Funding

This study was funded by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) and FAPERGS/CAPES (Fundação de Amparo à Pesquisa do Rio Grande do Sul/Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), which also granted the scholarship to the first author. Publication number 6049 of the Netherlands Institute of Ecology, NIOO-KNAW.

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M.L., L. R., and R.J. designed the study. M.L. together with A.S. collected the samples. M.L. and L.R. conducted the laboratory work. L.R., V.S.P., and L.N.L. performed the bioinformatic analysis of the sequence data. L.R., M.L., H.V., V.S.P., and E.K. wrote the manuscript with contributions of all authors. All authors have revised and approved the final manuscript.

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Correspondence to Luiz F. W. Roesch.

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Supplementary Table S1

Sample ID, treatment, total number of sequences and Good’s coverage using DNA- and RNA-based approach. (DOCX 100 kb)

Supplementary Table S2

Differential abundance analysis of soil microbial OTUs under a moisture gradient. (XLSX 139 kb)

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Lupatini, M., Suleiman, A.K.A., Jacques, R.J.S. et al. Moisture Is More Important than Temperature for Assembly of Both Potentially Active and Whole Prokaryotic Communities in Subtropical Grassland. Microb Ecol 77, 460–470 (2019). https://doi.org/10.1007/s00248-018-1310-1

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