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Community Structure and Function of Planktonic Crenarchaeota: Changes with Depth in the South China Sea

  • Environmental Microbiology
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Abstract

Marine Crenarchaeota represent a widespread and abundant microbial group in marine ecosystems. Here, we investigated the abundance, diversity, and distribution of planktonic Crenarchaeota in the epi-, meso-, and bathypelagic zones at three stations in the South China Sea (SCS) by analysis of crenarchaeal 16S rRNA gene, ammonia monooxygenase gene amoA involved in ammonia oxidation, and biotin carboxylase gene accA putatively involved in archaeal CO2 fixation. Quantitative PCR analyses indicated that crenarchaeal amoA and accA gene abundances varied similarly with archaeal and crenarchaeal 16S rRNA gene abundances at all stations, except that crenarchaeal accA genes were almost absent in the epipelagic zone. Ratios of the crenarchaeal amoA gene to 16S rRNA gene abundances decreased ~2.6 times from the epi- to bathypelagic zones, whereas the ratios of crenarchaeal accA gene to marine group I crenarchaeal 16S rRNA gene or to crenarchaeal amoA gene abundances increased with depth, suggesting that the metabolism of Crenarchaeota may change from the epi- to meso- or bathypelagic zones. Denaturing gradient gel electrophoresis profiling of the 16S rRNA genes revealed depth partitioning in archaeal community structures. Clone libraries of crenarchaeal amoA and accA genes showed two clusters: the “shallow” cluster was exclusively derived from epipelagic water and the “deep” cluster was from meso- and/or bathypelagic waters, suggesting that niche partitioning may take place between the shallow and deep marine Crenarchaeota. Overall, our results show strong depth partitioning of crenarchaeal populations in the SCS and suggest a shift in their community structure and ecological function with increasing depth.

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References

  1. Agogué H, Brink M, Dinasquet J, Herndl GJ (2008) Major gradients in putatively nitrifying and non-nitrifying archaea in the deep North Atlantic. Nature 456:788–791

    Article  PubMed  Google Scholar 

  2. Arístegui J, Gasol JM, Duarte CM, Herndl GJ (2009) Microbial oceanography of the dark ocean’s pelagic realm. Limnol Oceanogr 54:1501–1529

    Article  Google Scholar 

  3. Auguet JC, Borrego CM, Baneras L, Casamayor EO (2008) Fingerprinting the genetic diversity of the biotin carboxylase gene (accC) in aquatic ecosystems as a potential marker for studies of carbon dioxide assimilation in the dark. Environ Microbiol 10:2527–2536

    Article  PubMed  CAS  Google Scholar 

  4. Bano N, Ruffin S, Ransom B, Hollibaugh JT (2004) Phylogenetic composition of Arctic Ocean archaeal assemblages and comparison with Antarctic assemblages. Appl Environ Microbiol 70:781–789

    Article  PubMed  CAS  Google Scholar 

  5. Beman JM, Roberts KJ, Wegley L, Rohwer F, Francis CA (2007) Distribution and diversity of archaeal ammonia monooxygenase genes associated with corals. Appl Environ Microbiol 73:5642–5647

    Article  PubMed  CAS  Google Scholar 

  6. Beman JM, Popp BN, Francis CA (2008) Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J 2:429–441

    Article  PubMed  CAS  Google Scholar 

  7. Beman JM, Sachdeva R, Fuhrman JA (2010) Population ecology of nitrifying archaea and bacteria in the Southern California Bight. Environ Microbiol 12:1282–1292

    Article  PubMed  CAS  Google Scholar 

  8. Berg IA, Kockelkorn D, Buckel W, Fuchs G (2007) A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in archaea. Science 318:1782–1786

    Article  PubMed  CAS  Google Scholar 

  9. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252

    Article  PubMed  CAS  Google Scholar 

  10. Carpenter JH (1965) The Chesapeake Bay Institute technique for the Winkler dissolved oxygen method. Limnol Oceanogr 10:141–143

    Article  CAS  Google Scholar 

  11. Chen CTA, Wang SL, Wang BJ, Pai SC (2001) Nutrient budgets for the South China Sea basin. Mar Chem 75:281–300

    Article  CAS  Google Scholar 

  12. Church MJ, Wai B, Karl DM, DeLong EF (2010) Abundances of crenarchaeal amoA genes and transcripts in the Pacific Ocean. Environ Microbiol 12:679–688

    Article  PubMed  CAS  Google Scholar 

  13. Crump BC, Baross JA (2000) Archaeaplankton in the Columbia River, its estuary and the adjacent coastal ocean, USA. FEMS Microbiol Ecol 31:231–239

    Article  PubMed  CAS  Google Scholar 

  14. Dang H, Li J, Zhang X, Li T, Tian F, Jin W (2009) Diversity and spatial distribution of amoA-encoding archaea in the deep-sea sediments of the tropical West Pacific Continental Margin. J Appl Microbiol 106:1482–1493

    Article  PubMed  CAS  Google Scholar 

  15. Dang H, Luan XW, Chen R, Zhang X, Guo L, Klotz MG (2010) Diversity, abundance and distribution of amoA-encoding archaea in deep-sea methane seep sediments of the Okhotsk Sea. FEMS Microbiol Ecol 72:370–385

    Article  PubMed  CAS  Google Scholar 

  16. De Corte D, Yokokawa T, Varela MM, Agogue H, Herndl GJ (2009) Spatial distribution of bacteria and archaea and amoA gene copy numbers throughout the water column of the Eastern Mediterranean Sea. ISME J 3:147–158

    Article  PubMed  Google Scholar 

  17. de la Torre JR, Walker CB, Ingalls AE, Konneke M, Stahl DA (2008) Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10:810–818

    Article  PubMed  Google Scholar 

  18. DeLong EF (1992) Archaea in coastal marine environment. Proc Natl Acad Sci USA 89:5685–5689

    Article  PubMed  CAS  Google Scholar 

  19. DeLong EF, Wu KY, Prhelin BB, Jovine RV (1994) High abundance of archaea in Antarctic marine picoplankton. Nature 371:695–697

    Article  PubMed  CAS  Google Scholar 

  20. Ettema TJG, Andersson SGE (2008) Comment on “A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in archaea”. Science 321:342b

    Article  Google Scholar 

  21. Falster DS, Warton DI, Wright IJ (2006) SMATR: Standardised major axis tests and routines, ver 2.0. Available at: http://www.bio.mq.edu.au/ecology/SMATR

  22. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102:14683–14688

    Article  PubMed  CAS  Google Scholar 

  23. Fuhrman JA, McCallum K, Davis AA (1992) Novel major archaebacterial group from marine planton. Nature 356:148–149

    Article  PubMed  CAS  Google Scholar 

  24. Fuhrman JA, Davis AA (1997) Widespread archaea and novel bacteria from the deep sea as shown by 16S rRNA gene sequences. Mar Ecol Prog Ser 150:275–285

    Article  Google Scholar 

  25. Galand PE, Lovejoy C, Hamilton AK, Ingram RG, Pedneault E, Carmack EC (2009) Archaeal diversity and a gene for ammonia oxidation are coupled to oceanic circulation. Environ Microbiol 11:971–980

    Article  PubMed  Google Scholar 

  26. Garcia-Martinez J, Rodriguez-Valera F (2000) Microdiversity of uncultured marine prokaryotes: the SAR11 cluster and the marine archaea of group I. Mol Ecol 9:935–948

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  28. Hallam SJ, Mincer TJ, Schleper C, Preston CM, Roberts K, Richardson PM, DeLong EF (2006) Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol 4:e95

    Article  PubMed  Google Scholar 

  29. Hansman RL, Griffin S, Watson JT, Druffel ERM, Ingalls AE, Pearson A, Aluwihare LI (2009) The radiocarbon signature of microorganisms in the mesopelagic ocean. Proc Natl Acad Sci USA 106:6513–6518

    Article  PubMed  CAS  Google Scholar 

  30. Herfort L, Schouten S, Abbas B, Veldhuis MJW, Coolen MJL, Wuchter C, Boon JP, Herndl GJ, Damste JSS (2007) Variations in spatial and temporal distribution of archaea in the North Sea in relation to environmental variables. FEMS Microbiol Ecol 62:242–257

    Article  PubMed  CAS  Google Scholar 

  31. Herndl GJ, Reinthaler T, Teira E, van Aken H, Veth C, Pernthaler A, Pernthaler J (2005) Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean. Appl Environ Microbiol 71:2303–2309

    Article  PubMed  CAS  Google Scholar 

  32. Hu A, Yao T, Jiao N, Liu Y, Yang Z, Liu X (2010) Community structures of ammonia-oxidising archaea and bacteria in high-altitude lakes on the Tibetan Plateau. Freshwat Biol 55:2375–2390

    CAS  Google Scholar 

  33. Ingalls AE, Shah SR, Hansman RL, Aluwihare LI, Santos GM, Druffel ERM, Pearson A (2006) Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc Natl Acad Sci USA 103:6442–6447

    Article  PubMed  CAS  Google Scholar 

  34. Jia ZJ, Conrad R (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11:1658–1671

    Article  PubMed  CAS  Google Scholar 

  35. Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

    Article  PubMed  Google Scholar 

  36. Kalanetra KM, Bano N, Hollibaugh JT (2009) Ammonia-oxidizing archaea in the Arctic Ocean and Antarctic coastal waters. Environ Microbiol 11:2434–2445

    Article  PubMed  CAS  Google Scholar 

  37. Karner MB, DeLong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507–510

    Article  PubMed  CAS  Google Scholar 

  38. Konstantinidis KT, Braff J, Karl DM, DeLong EF (2009) Comparative metagenomic analysis of a microbial community from 4000 m at Station ALOHA in the North Pacific Subtropical Gyre. Appl Environ Microbiol 75:5345–5355

    Article  PubMed  CAS  Google Scholar 

  39. Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529

    Article  PubMed  CAS  Google Scholar 

  40. López-García P, Moreira D, López-Lopez A, Rodriguez-Valera F (2001) A novel haloarchaeal-related lineage is widely distributed in deep oceanic regions. Environ Microbiol 3:72–78

    Article  PubMed  Google Scholar 

  41. La Cono V, Smedile F, Ferrer M, Golyshin PN, Giuliano L, Yakimov MM (2010) Genomic signatures of fifth autotrophic carbon assimilation pathway in bathypelagic Crenarchaeota. Microb Biotechnol 3:595–606

    Article  PubMed  Google Scholar 

  42. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    Article  PubMed  CAS  Google Scholar 

  43. Liu B, Ye GB, Wang FP, Bell R, Noakes J, Short T, Zhang CL (2009) Community structure of archaea in the water column above gas hydrates in the Gulf of Mexico. Geomicrobiol J 26:363–369

    Article  CAS  Google Scholar 

  44. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar BA, Lai T, Steppi S, Jobb G, Forster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, Konig A, Liss T, Lussmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  PubMed  CAS  Google Scholar 

  45. Magalhaes CM, Machado A, Bordalo AA (2009) Temporal variability in the abundance of ammonia-oxidizing bacteria vs. archaea in sandy sediments of the Douro River estuary, Portugal. Aquat Microb Ecol 56:13–23

    Article  Google Scholar 

  46. Massana R, DeLong EF, Pedros-Alio C (2000) A few cosmopolitan phylotypes dominate planktonic archaeal assemblages in widely different oceanic provinces. Appl Environ Microbiol 66:1777–1787

    Article  PubMed  CAS  Google Scholar 

  47. Mincer TJ, Church MJ, Taylor LT, Preston C, Karl DM, DeLong EF (2007) Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ Microbiol 9:1162–1175

    Article  PubMed  CAS  Google Scholar 

  48. Nakagawa T, Mori K, Kato C, Takahashi R, Tokuyama T (2007) Distribution of cold-adapted ammonia-oxidizing microorganisms in the deep-ocean of the northeastern Japan Sea. Microbes Environ 22:365–372

    Article  Google Scholar 

  49. Nicol GW, Tscherko D, Embley TM, Prosser JI (2005) Primary succession of soil Crenarchaeota across a receding glacier foreland. Environ Microbiol 7:337–347

    Article  PubMed  CAS  Google Scholar 

  50. Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10:2966–2978

    Article  PubMed  CAS  Google Scholar 

  51. Øvreås L, Forney L, Daae FL, Torsvik V (1997) Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63:3367–3373

    PubMed  Google Scholar 

  52. Park BJ, Park SJ, Yoon DN, Schouten S, Damste JSS, Rhee SK (2010) Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl Environ Microbiol 76:7575–7587

    Article  PubMed  CAS  Google Scholar 

  53. Purkhold U, Pommerening-Roser A, Juretschko S, Schmid MC, Koops HP, Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: Implications for molecular diversity surveys. Appl Environ Microbiol 66:5368–5382

    Article  PubMed  CAS  Google Scholar 

  54. Reinthaler T, van Aken HM, Herndl GJ (2010) Major contribution of autotrophy to microbial carbon cycling in the deep North Atlantic's interior. Deep-Sea Res Pt II 57:1572–1580

    Article  CAS  Google Scholar 

  55. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  56. Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712

    PubMed  CAS  Google Scholar 

  57. Santoro AE, Casciotti KL, Francis CA (2010) Activity, abundance and diversity of nitrifying archaea and bacteria in the central California current. Environ Microbiol 12:1989–2006

    Article  PubMed  CAS  Google Scholar 

  58. Schleper C, Jurgens G, Jonuscheit M (2005) Genomic studies of uncultivated archaea. Nat Rev Microbiol 3:479–488

    Article  PubMed  CAS  Google Scholar 

  59. Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506

    Article  PubMed  CAS  Google Scholar 

  60. Schloss PD, Handelsman J (2006) Introducing SONS, a tool for operational taxonomic unit-based comparisons of microbial community memberships and structures. Appl Environ Microbiol 72:6773–6779

    Article  PubMed  CAS  Google Scholar 

  61. Shaw PT, Chao SY, Liu KK, Pai SC, Liu CT (1996) Winter upwelling off Luzon in the north-eastern South China Sea. J Geophys Res 101:16435–16488

    Article  Google Scholar 

  62. Stahl DA, Amann R (1991) Development and application of nucleic acid probes. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics, vol 8, Wiley. Chichester, England, pp 205–248

    Google Scholar 

  63. Spang A, Hatzenpichler R, Brochier-Armanet C, Rattei T, Tischler P, Spieck E, Streit W, Stahl DA, Wagner M, Schleper C (2010) Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol 18:331–340

    Article  PubMed  CAS  Google Scholar 

  64. Swofford DL (2003) PAUP*, phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland

    Google Scholar 

  65. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 7:1985–1995

    Article  PubMed  CAS  Google Scholar 

  66. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu DY, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74

    Article  PubMed  CAS  Google Scholar 

  67. Walker CB, de la Torre JR, Klotz MG, Urakawa H, Pinel N, Arp DJ, Brochier-Armanet C, Chain PSG, Chan PP, Gollabgir A (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA 107:8818–8823

    Article  PubMed  CAS  Google Scholar 

  68. Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291

    Article  PubMed  Google Scholar 

  69. Wong GTF, Ku TL, Mulholland M, Tseng CM, Wang DP (2007) The SouthEast Asian time-series study (SEATS) and the biogeochemistry of the South China Sea–an overview. Deep-Sea Res Pt II 54:1434–1447

    Article  CAS  Google Scholar 

  70. Wuchter C, Abbas B, Coolen MJL, Herfort L, van Bleijswijk J, Timmers P, Strous M, Teira E, Herndl GJ, Middelburg JJ, Schouten S, Damsté JSS (2006) Archaeal nitrification in the ocean. Proc Natl Acad Sci USA 103:12317–12322

    Article  PubMed  CAS  Google Scholar 

  71. Yakimov MM, La Cono V, Denaro R, D'Auria G, Decembrini F, Timmis KN, Golyshin PN, Giuliano L (2007) Primary producing prokaryotic communities of brine, interface and seawater above the halocline of deep anoxic lake L'Atalante, Eastern Mediterranean Sea. ISME J 1:743–755

    Article  PubMed  CAS  Google Scholar 

  72. Yakimov MM, Conoa VL, Denaroa R (2009) A first insight into the occurrence and expression of functional amoA and accA genes of autotrophic and ammonia-oxidizing bathypelagic Crenarchaeota of Tyrrhenian Sea. Deep-Sea Res Pt II 56:748–754

    Article  CAS  Google Scholar 

  73. Yakimov MM, La Cono V, Smedile F, DeLuca TH, Juarez S, Ciordia S, Fernandez M, Albar JP, Ferrer M, Golyshin PN, Giuliano L (2011) Contribution of crenarchaeal autotrophic ammonia oxidizers to the dark primary production in Tyrrhenian deep waters (Central Mediterranean Sea). ISME J. doi:10.1038/ismej.2010.1197

    PubMed  Google Scholar 

  74. Zhang M (2009) Productivity and nutrient dynamics in the modern South China Sea. In: Wang P, Li Q (eds) The South China Sea. Paleooceanography and sedimentology. Springer, New York, pp 439–457

    Google Scholar 

  75. Zhang Y, Sintes E, Chen MN, Zhang Y, Dai MH, Jiao NZ, Herndl GJ (2009) Role of mesoscale cyclonic eddies in the distribution and activity of archaea and bacteria in the South China Sea. Aquat Microb Ecol 56:65–79

    Article  Google Scholar 

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Acknowledgments

We thank the captain and crew of the RV “Dongfanghong” #2, L. Wang and R. Zong for assistance in collecting the samples, Z. Y. Sun and J. Zhu for providing the temperature and salinity data, and M. H. Dai for providing the dissolved oxygen data. The manuscript benefits from careful reading and constructive comments by James T. Hollibaugh. N. Jiao was supported by MOST (2007CB815900), NSFC (40632013 and 40821063), and SOA (200805068). C. Zhang was supported by NSFC (91028005) and the State Key Laboratory of Marine Geology Lecturer Professorship at Tongji University. A. Hu was supported by the MEL Young Scientist Visiting Fellowship (MELRS1026) from the State Key Laboratory of Marine Environmental Science at Xiamen University.

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Table S1

Thermocycling condition and efficiency of individual qPCR assay in this study (DOC 39 kb)

Table S2

Summary for qPCR estimates of gene abundance in the samples from the SCS (DOC 71 kb)

Table S3

Summary for qPCR estimates of gene abundance in the particle-associated samples from station Y23 in the SCS (DOC 31 kb)

Fig. S1

Theta-S diagram of the water masses at the sampling stations S2, Z97 and Y23. Locations of water samples used to qPCR analysis are marked with symbols (S2, circles; Z97, rectangles; and Y23, triangles) and samples used to the clone library and DGGE analysis are indicated by arrows. The epipelagia is defined as <200 m depth, the mesopelagia 200–1,000 m depth, and the bathypelagia >1,000 m depth (Arístegui et al. 2009) (DOC 236 kb)

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Hu, A., Jiao, N. & Zhang, C.L. Community Structure and Function of Planktonic Crenarchaeota: Changes with Depth in the South China Sea. Microb Ecol 62, 549–563 (2011). https://doi.org/10.1007/s00248-011-9866-z

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