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Effects of Culturing on the Population Structure of a Hyperthermophilic Virus

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Abstract

The existence of a culturing bias has long been known when sampling organisms from the environment. This bias underestimates microbial diversity and does not accurately reflect the most ecologically relevant species. Until now no study has examined the effects of culture bias on viral populations. We have employed culture-independent methods to assess the diversity of Sulfolobus spindle–shaped viruses (SSVs) from extremely hyperthermal environments. This diversity is then compared to the viral diversity of cultured samples. We detected a clear culturing bias between environmental samples and cultured isolates. This is the first study identifying a culture bias in a viral population.

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References

  1. RI Amann W Ludwig KH Schleifer (1995) ArticleTitlePhylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59 143–169 Occurrence Handle1:CAS:528:DyaK2MXkvVGmurk%3D Occurrence Handle7535888

    CAS  PubMed  Google Scholar 

  2. SM Barns CF Delwiche JD Palmer NR Pace (1996) ArticleTitlePerspectives on archaeal diversity, thermophily, and monophyly from environmental rRNA sequences. Proc Natl Acad Sci USA 93 9188–9193 Occurrence Handle10.1073/pnas.93.17.9188 Occurrence Handle1:CAS:528:DyaK28Xlt1Cntrc%3D Occurrence Handle8799176

    Article  CAS  PubMed  Google Scholar 

  3. SM Barns RE Fundyga MW Jeffries NR Pace (1994) ArticleTitleRemarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc Natl Acad Sci USA 91 1609–1613 Occurrence Handle1:CAS:528:DyaK2c**tFanurw%3D Occurrence Handle7510403

    CAS  PubMed  Google Scholar 

  4. DG Higgins JD Thompson TJ Gibson (1996) ArticleTitleUsing CLUSTAL for multiple sequence alignments. Methods Enzymol 266 383–402 Occurrence Handle1:CAS:528:DyaK28Xltl2nt7w%3D Occurrence Handle8743695

    CAS  PubMed  Google Scholar 

  5. JP Huelsenbeck F Ronquist (2001) ArticleTitleMRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17 745–755 Occurrence Handle10.1093/bioinformatics/17.8.754

    Article  Google Scholar 

  6. P Hugenholtz C Pitulle KL Hershberger NR Pace (1998) ArticleTitleNovel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180 366–376 Occurrence Handle1:CAS:528:DyaK1cXlsVaqsA%3D%3D Occurrence Handle9440526

    CAS  PubMed  Google Scholar 

  7. AL Hughes R Friedman (2003) ArticleTitleGenome-wide survey for genes horizontally transferred from cellular organisms to baculoviruses. Mol Biol Evol 20 979–978

    Google Scholar 

  8. F Jeanmougin JD Thompson M Gouy DG Higgins TJ Gibson (1998) ArticleTitleMultiple sequence alignment with Clustal X. Trends Biochem Sci 23 403–405 Occurrence Handle10.1016/S0968-0004(98)01285-7 Occurrence Handle1:CAS:528:DyaK1cXntlansLg%3D Occurrence Handle9810230

    Article  CAS  PubMed  Google Scholar 

  9. KE Nelson RA Clayton SR Gill ML Gwinn RJ Dodson DH Haft EK Hickey JD Peterson WC Nelson KA Ketchum L McDonald TR Utterback JA Malek KD Linher MM Garrett AM Stewart MD Cotton MS Pratt CA Phillips D Richardson J Heidelberg GG Sutton RD Fleischmann JA Eisen CM Fraser et al. (1999) ArticleTitleEvidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima. Nature 399 323–329 Occurrence Handle10.1038/20601 Occurrence Handle1:CAS:528:DyaK1MXjs1WnsLo%3D Occurrence Handle10360571

    Article  CAS  PubMed  Google Scholar 

  10. P Palm C Schleper B Grampp S Yeats P McWilliam WD Reiter W Zillig (1991) ArticleTitleComplete nucleotide sequence of the virus SSV1 of the archaebacterium Sulfolobus shibatae. Virology 185 242–250

    Google Scholar 

  11. X Peng H Blum Q She S Mallok K Brugger RA Garrett W Zilling D Pragishvili (2001) ArticleTitleSequences and replication of genomes of the archaeal rudiviruses SIRV1 and SIRV2: relationships to the archaeal lipothrixvirus SIFV and some eukaryal viruses. Virology 291 226–234 Occurrence Handle10.1006/viro.2001.1190 Occurrence Handle1:CAS:528:DC%2BD38**t1yksg%3D%3D Occurrence Handle11878892

    Article  CAS  PubMed  Google Scholar 

  12. D Posada KA Crandall (1998) ArticleTitleMODELTEST: testing the model of DNA substitution. Bioinformatics 14 817–818 Occurrence Handle10.1093/bioinformatics/14.9.817 Occurrence Handle1:CAS:528:DyaK1MXktlCltw%3D%3D Occurrence Handle9918953

    Article  CAS  PubMed  Google Scholar 

  13. R Rachel M Bettstetter BP Hedlund M Haring A Kessler KO Stetter D Prangishvili (2002) ArticleTitleRemarkable morphological diversity of viruses and virus-like particles in hot terrestrial environments. Arch Virol 147 2419–2429 Occurrence Handle10.1007/s00705-002-0895-2 Occurrence Handle1:CAS:528:DC%2BD38XpsFOmsbY%3D Occurrence Handle12491107

    Article  CAS  PubMed  Google Scholar 

  14. G Rice K Stedman J Snyder B Wiedenheft D Willits S Brumfield T McDermott MJ Young (2001) ArticleTitleViruses from extreme thermal environments. Proc Natl Acad Sci USA 98 13341–13345

    Google Scholar 

  15. Q She RK Singh F Confalonieri Y Zivanovic G Allard MJ Awayez CC-Y Chan-Weiher IG Clausen BA Curtis AD Moors G Erauso C Fletcher PMK Gordon IH-d Jong AC Jeffries CJ Kozera N Medina X Peng HP Thi-Ngoc P Redder ME Schenk C Theriault N Tolstrup RL Charlebois WF Doolittle M Duguet T Gaasterland RA Garrett MA Ragan CW Sensen JVd Oost (2001) ArticleTitleThe complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci USA 98 7835–7840 Occurrence Handle10.1073/pnas.141222098 Occurrence Handle1:CAS:528:DC%2BD3MXlt1Kntr0%3D Occurrence Handle11427726

    Article  CAS  PubMed  Google Scholar 

  16. KM Stedman C Schleper E Rumpf W Zillig (1999) ArticleTitleGenetic requirements for the function of the archaeal virus SSV1 in Sulfolobus solfataricus: construction and testing of viral shuttle vectors. Genetics 152 1397–1405 Occurrence Handle1:CAS:528:DyaK1MXlslSrtL0%3D Occurrence Handle10430570

    CAS  PubMed  Google Scholar 

  17. KM Stedman Q She H Phan HP Arnold I Holz RA Garrett W Zillig (2003) ArticleTitleRelationships between fuselloviruses infecting the extremely thermophilic archaeon Sulfolobus: SSV1 and SSV2. Res Microbiol 154 295–302 Occurrence Handle10.1016/S0923-2508(03)00074-3 Occurrence Handle1:CAS:528:DC%2BD3sXkt1ymurk%3D Occurrence Handle12798235

    Article  CAS  PubMed  Google Scholar 

  18. MB Sullivan JB Waterbury SW Chisholm (2003) ArticleTitleCyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424 1047–1051 Occurrence Handle10.1038/nature01929 Occurrence Handle1:CAS:528:DC%2BD3sXmslSjt74%3D Occurrence Handle12944965

    Article  CAS  PubMed  Google Scholar 

  19. Swofford, DL (2002) PAUP*4.0 Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4 beta 10 ed., Sinauer Associates, Sunderlund, MA

  20. DM Ward MJ Ferris SC Nold MM Bateson (1998) ArticleTitleA natural view of microbial biodiversity within hot spring cyanobacterial mat communities. Microbiol Mol Biol Rev 62 1353–1370 Occurrence Handle1:STN:280:DyaK1M%2FlvVWnsg%3D%3D Occurrence Handle9841675

    CAS  PubMed  Google Scholar 

  21. DM Ward R Weller MM Bateson (1990) ArticleTitle16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature 345 63–65 Occurrence Handle10.1038/345063a0 Occurrence Handle1:CAS:528:DyaK3cXktlOltbo%3D Occurrence Handle1691827

    Article  CAS  PubMed  Google Scholar 

  22. B Wiedenheft K Stedman F Roberto D Willits A-K Gleske L Zoeller J Snyder T Douglas M Young (2004) ArticleTitleComparative genomic analysis of hyperthermophilic archaeal fuselloviridae viruses. J Virol 78 1954–1961 Occurrence Handle10.1128/JVI.78.4.1954-1961.2004 Occurrence Handle1:CAS:528:DC%2BD2cXhtFKns74%3D Occurrence Handle14747560

    Article  CAS  PubMed  Google Scholar 

  23. S Yeats P McWilliam W Zillig (1982) ArticleTitleA plasmid in the archaebacterium Sulfolobus acidocaldarius. EMBO J 1 1035–1038 Occurrence Handle1:CAS:528:DyaL3sXhtVyn

    CAS  Google Scholar 

  24. W Zillig A Kletzin C Schleper I Holz D Janekovic J Hain M Lanzedorfer JK Kristjansson (1994) ArticleTitleScreening for Sulfolobales, their plasmids, and their viruses in Icelandic solfataras. Syst Appl Microbiol 16 609–628 Occurrence Handle1:CAS:528:DyaK2cXksFeks7g%3D

    CAS  Google Scholar 

  25. W Zillig KO Stetter S Wunderl W Schulz H Preiss H Scholz (1980) ArticleTitleThe Sulfolobus–“Caldariella” group: taxonomy on the basis of the structure of DNA-dependent RNA polymerases. Arch Microbiol 125 259–269 Occurrence Handle1:CAS:528:DyaL3c**tFWnurY%3D

    CAS  Google Scholar 

Download references

Acknowledgments

We thank Matthew Lavin and Mary Bateson for critically reading this manuscript. This research was conducted with permission from Yellowstone National Park research permit YELL-05090. This work is supported by grants from the National Science Foundation (MCB01322156) and the National Aeronautics and Space Administration (NAG5-8807).

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Correspondence to M.J. Young.

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Snyder, J., Spuhler, J., Wiedenheft, B. et al. Effects of Culturing on the Population Structure of a Hyperthermophilic Virus. Microb Ecol 48, 561–566 (2004). https://doi.org/10.1007/s00248-004-0246-9

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  • DOI: https://doi.org/10.1007/s00248-004-0246-9

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