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Microbial Ecology

, Volume 77, Issue 2, pp 460–470 | Cite as

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

  • Manoeli Lupatini
  • Afnan K. A. Suleiman
  • Rodrigo J. S. Jacques
  • Leandro N. Lemos
  • Victor S. Pylro
  • Johannes A. Van Veen
  • Eiko E. Kuramae
  • Luiz F. W. RoeschEmail author
Soil Microbiology

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.

Keywords

16S rRNA gene 16S rRNA transcript Seasonality Assembly process Microbial ecology 

Notes

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.

Author Contributions

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.

Funding Information

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.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2018_1310_MOESM1_ESM.docx (55 kb)
Fig S1 (DOCX 54 kb)
248_2018_1310_MOESM2_ESM.docx (101 kb)
Supplementary Table S1 Sample ID, treatment, total number of sequences and Good’s coverage using DNA- and RNA-based approach. (DOCX 100 kb)
248_2018_1310_MOESM3_ESM.xlsx (140 kb)
Supplementary Table S2 Differential abundance analysis of soil microbial OTUs under a moisture gradient. (XLSX 139 kb)

References

  1. 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 CrossRefGoogle Scholar
  2. 2.
    Stark JM, Firestone MK (1995) Mechanisms for soil moisture effects on activity of nitrifying bacteria. Appl Environ Microbiol 61:218–221Google Scholar
  3. 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 513:81–84CrossRefGoogle Scholar
  4. 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 CrossRefGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. 6.
    Young IM (2004) Interactions and self-organization in the soil-microbe complex. Science 304:1634–1637.  https://doi.org/10.1126/science.1097394 CrossRefGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. 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. 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 CrossRefGoogle Scholar
  14. 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 CrossRefGoogle Scholar
  15. 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 7:1310–1321CrossRefGoogle Scholar
  16. 16.
    Chase JM (2007) Drought mediates the importance of stochastic community assembly. Proc Natl Acad Sci 104:17430–17434CrossRefGoogle Scholar
  17. 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. 18.
    Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505CrossRefGoogle Scholar
  19. 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;2Google Scholar
  20. 20.
    Jones CM, Hallin S (2010) Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME J 4:633–641CrossRefGoogle Scholar
  21. 21.
    Stegen JC, Lin X, Konopka AE, Fredrickson JK (2012) Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J 6:1653–1664CrossRefGoogle Scholar
  22. 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 CrossRefGoogle Scholar
  23. 23.
    Roesch LFW, Vieira FCB, Pereira VA et al (2009) The Brazilian Pampa: a fragile biome. Diversity 1:182–198CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 25.
    Klute A (1986) Methods of soil analysis: part 1—physical and mineralogical methods. Soil Science Society of America, American Society of Agronomy, MadisonGoogle Scholar
  26. 26.
    Reinert DJ, Reichert JM (2006) Coluna de areia para medir a retenção de água no solo: protótipos e teste. Ciênc Rural 36:1931–1935CrossRefGoogle Scholar
  27. 27.
    da Silva FC (Ed.) (2009) Manual de análises químicas de solos, plantas e fertilizantes. Embrapa Informação Tecnológica; Rio de Janeiro: Embrapa Solos, BrasíliaGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 2011Google Scholar
  30. 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 CrossRefGoogle Scholar
  31. 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. 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 CrossRefGoogle Scholar
  33. 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 72:443–447CrossRefGoogle Scholar
  34. 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 CrossRefGoogle Scholar
  35. 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 CrossRefGoogle Scholar
  36. 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 CrossRefGoogle Scholar
  37. 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 CrossRefGoogle Scholar
  38. 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 CrossRefGoogle Scholar
  39. 39.
    R Development Core Team (2008) R: a language and environment for statistical computingGoogle Scholar
  40. 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 CrossRefGoogle Scholar
  41. 41.
    Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264CrossRefGoogle Scholar
  42. 42.
    Lemos et al (2011) Rethinking microbial diversity analysis in the hig.pdfGoogle Scholar
  43. 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 1–15Google Scholar
  44. 44.
    Oksanen J, Blanchet F G, Kindt R, et al (2015) Vegan: community ecology package. R package vegan, vers. 2.2–1Google Scholar
  45. 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;2Google Scholar
  46. 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. 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 CrossRefGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. 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 CrossRefGoogle Scholar
  50. 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 CrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 CrossRefGoogle Scholar
  53. 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 CrossRefGoogle Scholar
  54. 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 3:738–744CrossRefGoogle Scholar
  55. 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 9:946–957CrossRefGoogle Scholar
  56. 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 CrossRefGoogle Scholar
  57. 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. 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 CrossRefGoogle Scholar
  59. 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 CrossRefGoogle Scholar
  60. 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 CrossRefGoogle Scholar
  61. 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 CrossRefGoogle Scholar
  62. 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 CrossRefGoogle Scholar
  63. 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 CrossRefGoogle Scholar
  64. 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 CrossRefGoogle Scholar
  65. 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 CrossRefGoogle Scholar
  66. 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 CrossRefGoogle Scholar
  67. 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 CrossRefGoogle Scholar
  68. 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 CrossRefGoogle Scholar
  69. 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 4:337–345CrossRefGoogle Scholar
  70. 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 CrossRefGoogle Scholar
  71. 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

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Manoeli Lupatini
    • 1
  • Afnan K. A. Suleiman
    • 1
    • 2
  • Rodrigo J. S. Jacques
    • 1
  • Leandro N. Lemos
    • 3
  • Victor S. Pylro
    • 4
  • Johannes A. Van Veen
    • 2
  • Eiko E. Kuramae
    • 2
  • Luiz F. W. Roesch
    • 5
    Email author
  1. 1.Departamento de Solos, Programa de Pós-graduação em Ciência do SoloUniversidade Federal de Santa MariaSanta MariaBrazil
  2. 2.Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW)WageningenThe Netherlands
  3. 3.Laboratório de Biologia Molecular e Celular, Centro de Energia Nuclear na Agricultura CENAUniversidade de São Paulo USPPiracicabaBrazil
  4. 4.Department of BiologyFederal University of Lavras – UFLALavrasBrazil
  5. 5.Centro Interdisciplinar de Pesquisas em Biotecnologia – CIP-BiotecUniversidade Federal do PampaSão GabrielBrazil

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