Antonie van Leeuwenhoek

, Volume 101, Issue 1, pp 13–20 | Cite as

A call to arms for systematists: revitalising the purpose and practises underpinning the description of novel microbial taxa

  • Iain C. Sutcliffe
  • Martha E. Trujillo
  • Michael Goodfellow
Perspective

Abstract

Prokaryotic systematics is a fundamentally important discipline that provides a framework for the activities of all microbiologists. Here we propose that the field has become mired in a sea of perceived rules and regulations, many of which stipulate what is considered ‘sufficient’ for the phenotypic characterisation of novel prokaryotic taxa. Importantly, we argue also that the principles and practise of prokaryotic systematics have not yet fully embraced the revolution in biological understanding that has occurred through the availability of huge numbers of whole genome sequences. We therefore propose that a significant reappraisal of the procedures used to describe novel prokaryotic taxa is needed, including the likely introduction of new publication formats. Urgent action is needed to revitalise the practise of prokaryotic systematics in order to maintain this discipline as an attractive career choice for twenty first century life scientists.

Keywords

Bacterial species Chemotaxonomy Microbial diversity Phylogeny Systematics Taxonomy 

References

  1. Achtman M, Wagner M (2008) Microbial diversity and the genetic nature of microbial species. Nature Rev Microbiol 6:431–440Google Scholar
  2. Adékambi T, Butler RW, Hanrahan F, Delcher AL, Drancourt M, Shinnick TM (2011) Core gene set as the basis of multilocus sequence analysis of the subclass Actinobacteridae. PLOS One 6:e14792PubMedCrossRefGoogle Scholar
  3. Ball CA, Brazma A, Causton H, Chervitz S, Edgar R, Hingamp P, Matese JC, Parkinson H, Quackenbush J, Ringwald M, Sansone S-A, Sherlock G, Spellman P, Stoeckert C, Tateno Y, Taylor R, White J, Winegarden N (2004) Submission of microarray data to public repositories. PLOS Biol 2:e317PubMedCrossRefGoogle Scholar
  4. Butler-Wu SM, Sengupta DJ, Kittichotirat W, Matsen FA III, Bumgarner RE (2011) Genome sequence of a novel species, Propionibacterium humerusii. J Bacteriol 193:3678PubMedCrossRefGoogle Scholar
  5. Chun J, Lee J-H, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261PubMedCrossRefGoogle Scholar
  6. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P (2006) Toward automatic reconstruction of a highly evolved tree of life. Science 311:1283–1287PubMedCrossRefGoogle Scholar
  7. Coeyne T, Gevers D, van de Peer Y, Vandamme P, Swings J (2005) Towards a prokaryotic genomic taxonomy. FEMS Microbiol Rev 29:147–167Google Scholar
  8. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis 37:D141–D145Google Scholar
  9. Cowan ST (1965) Principles and practise of bacterial taxonomy—a forward look. J Gen Microbiol 39:143–158PubMedCrossRefGoogle Scholar
  10. Curtis TP, Sloan WT, Scannell JW (2002) Estimating prokaryotic diversity and its limits. Proc Nat Acad Sci USA 99:10494–10499PubMedCrossRefGoogle Scholar
  11. Delmont TO, Robe P, Cecillon S, Clark IM, Constancias F, Simonet P, Hirsch PR, Vogel TM (2011) Acessing the soil metagenome for studies of microbial diversity. Appl Env Microbiol 77:1315–1324CrossRefGoogle Scholar
  12. Donati C, Hiller NL, Tettelin H, Muzzi A, Croucher NJ, Angiuoli SV, Oggioni M, Dunning Hotopp JC, Hu FZ, Riley DR, Covacci A, Mitchell TJ, Bentley SD, Kilian M, Ehrlich GD, Rappuoli R, Moxon ER, Masignani V (2010) Structure and dynamics of the pan-genome of Streptococcus pneumoniae and closely related species. Genome Biol 11:R107PubMedCrossRefGoogle Scholar
  13. Dykhuizen DE (1998) Santa Rosalia revisited: why are there so mnay species of bacteria? Antonie van Leeuwenhoek 73:25–33PubMedCrossRefGoogle Scholar
  14. Felis GE, Dellaglio F (2007) On species descriptions based on a single strain: proposal to introduce the status species proponenda (sp. pr.). Int J Syst Evol Microbiol 57:2185–2187PubMedCrossRefGoogle Scholar
  15. Field D, Amaral-Zettler L, Cochrane G, Cole JR, Dawyndt P, Garrity GM, Gilbert J, Glöckner FO, Hirschman L, Karsch-Mizrachi I, Klenk H-P, Knight R, Kottmann R, Kyrpides N, Meyer F, San Gil I, Sansone S-A, Schriml LM, Sterk P, Tatusova T, Ussery DW, White O, Wooley J (2011) The genomics standards consortium. PLOS Biol 9:e1001088PubMedCrossRefGoogle Scholar
  16. Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, Stackebrandt E, Van de Peer Y, Vandamme P, Thompson FL, Swings J (2005) Re-evaluating prokaryotic species. Nature Rev Microbiol 3:733–739CrossRefGoogle Scholar
  17. Gilbert JA, Meyer F, Antonoploulos D, Balaji P, Brown CT, Brown CT, Desai N, Eisen JA, Evers D, Feng W, Huson D, Jansson J, Knight R, Knight J, Kolker E, Kostantindis K, Kostka J, Kyrpides N, Mackelprang R, McHardy A, Quince C, Raes J, Sczyrba A, Shade A, Stevens R (2010) Meeting report. The terabase metagenomics workshop and the vision of an earth microbiome project. Stand in Genom Sci 3:243–248CrossRefGoogle Scholar
  18. Goodfellow M, Fiedler H-P (2010) A guide to successful bio prospecting: informed by actinobacterial systematics. Antonie van Leeuwenhoek 98:119–142PubMedCrossRefGoogle Scholar
  19. Gupta RS, Shami A (2011) Molecular signatures for the Crenarchaeota and the Thaumarchaeota. Antonie van Leeuwenhoek 99:133–157PubMedCrossRefGoogle Scholar
  20. Gupta RS, Vaibhav B (2011) Phylogeny and molecular signatures for the phylum Thermotogae and its subgroups. Antonie van Leeuwenhoek 100:1–34PubMedCrossRefGoogle Scholar
  21. Hanage WP, Frase C, Spratt BG (2006) Sequences, sequence clusters and bacterial species. Phil Trans R Soc B 361:1917–1927PubMedCrossRefGoogle Scholar
  22. Jensen P (2010) Linking species concepts to natural product discovery in the post-genomic era. J Ind Microbiol Biotechnol 37:219–224PubMedCrossRefGoogle Scholar
  23. Klenk H-P, Göker G (2010) En route to a genome-based classification of archaea and bacteria. Syst Appl Microbiol 33:175–182PubMedCrossRefGoogle Scholar
  24. Konstantinidis KT, Tiedje JM (2007) Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr Opin Microbiol 10:504–509PubMedCrossRefGoogle Scholar
  25. Lagesen K, Ussery DW, Wassenaar TM (2010) Genome update: the 1000th genome—a cautionary tale. Microbiology 156:603–608PubMedCrossRefGoogle Scholar
  26. Lefébure T, Stanhope MJ (2007) Evolution of the core and pan-genome of Streptococcus: positive selection, recombination, and genome composition. Genome Biol 8:R71PubMedCrossRefGoogle Scholar
  27. Maiden MCM (2006) Multilocus sequence typing of bacteria. Ann Rev Microbiol 60:561–588CrossRefGoogle Scholar
  28. Marcy Y, Ouverney C, Bik EM, Lösekann T, Ivanova N, Martin HG, Szeto E, Platt D, Hugenholtz P, Relamn DA, Quake SR (2007) Dissecting biological ‘dark matter’ with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc Nat Acad Sci USA 104:11889–11894PubMedCrossRefGoogle Scholar
  29. Mira A, Martín-Cuadrado AB, D’auria G, Rodríguez-Valera F (2010) The bacterial pan-genome: a new paradigm in microbiology. Int Microbiol 13:45–57PubMedGoogle Scholar
  30. Murray RGE, Stackebrandt E (1995) Taxonomic note: implementation of the provisional status Candidatus for incompletely described prokaryotes. Int J Syst Bacteriol 45:186–187PubMedCrossRefGoogle Scholar
  31. Pace NR (2009) Mapping the tree of life: progress and prospects. Microbiol Mol Biol Rev 73:565–576PubMedCrossRefGoogle Scholar
  32. Pérez-Núñez D, Briandet R, David B, Gautier C, Renault P, Hallet B, Hols P, Carballido-López R, Guédon E (2011) A new morphogenesis pathway in bacteria: unbalanced activity of cell wall synthesis machineries leads to coccus-to-rod transition and filamentation in ovococci. Mol Microbiol 79:759–771PubMedCrossRefGoogle Scholar
  33. Pruesse E, Quast C, Knittel K, Fuchs B, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196PubMedCrossRefGoogle Scholar
  34. Rappé MS, Giovannoni SJ (2003) The uncultured microbial majority. Ann Rev Microbiol 57:369–394CrossRefGoogle Scholar
  35. Rosselló-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67PubMedCrossRefGoogle Scholar
  36. Schleifer KH (2009) Classification of bacteria and archaea: past, present and future. Syst Appl Microbiol 32:533–542PubMedCrossRefGoogle Scholar
  37. Siegl A, Kamke J, Hochmuth T, Piel J, Richter M, Liang C, Dandekar T, Hentschel U (2011) Single-cell genomics reveals the lifestyle of Poribacteria, a candidate phylum symbiotically associated with marine sponges. ISME J 5:61–70PubMedCrossRefGoogle Scholar
  38. Skerman VBD, McGowan V, Sneath PHA (1980) Approved lists of bacterial names. Int J Syst Bacteriol 30:225–420CrossRefGoogle Scholar
  39. Sneath PHA (1995) 30 years of numerical taxonomy. System Biol 44:281–298Google Scholar
  40. Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155Google Scholar
  41. Stackebrandt E, Frederiksen W, Garrity GM, Grimont PAD, Kämpfer P, Maiden MCJ, Nesme X, Rosselló-Mora R, Swings J, Trüper HG, Vauterin L, Ward AC, Whitman WB (2002) Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J System Evol Microbiol 52:1043–1047CrossRefGoogle Scholar
  42. Staley JT (2010) Comprehending microbial diversity: the fourth goal of microbial taxonomy. Bulletin of BISMiS 1. http://www.bergeys.org/bismisbulletintoc.html
  43. Sutcliffe IC (2010) A phylum level perspective on bacterial cell envelope architecture. Trends Microbiol 18:464–470PubMedCrossRefGoogle Scholar
  44. Taylor CF, Paton NW, Lilley KS, Binz P-A, Julian RK Jr, Jones AR, Zhu W, Apweiler R, Aebersold R, Deutsch EW, Dunn MJ, Heck AJR, Leitner A, Macht M, Mann M, Martens L, Neubert TA, Patterson SD, Ping P, Seymour SL, Souda P, Tsugita A, Vandekerckhove J, Vondriska TM, Whitelegge JP, Wilkins MR, Xenarios I, Yates JR III, Hermjakob H (2007) The minimum information about a proteomics experiment (MIAPE). Nature Biotech 25:887–893CrossRefGoogle Scholar
  45. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, DeBoy RT, Davidsen TM, Mora M, Scarselli M, Ros IMY, Peterson JD, Hauser CR, Sundaram JP, Nelson WC, Madupu R, Brinkac LM, Dodson RJ, Rosovitz MJ, Sullivan SA, Daugherty SC, Haft DH, Selengut J, Gwinn ML, Zhou LW, Zafar N, Khouri H, Radune D, Dimitrov G, Watkins K, O’Connor KJB, Smith S, Utterback TR, White O, Rubens CE, Grandi G, Madoff LC, Kasper DL, Telford JL, Wessels MR, Rappuoli R, Fraser CM (2005) Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial ‘pan-genome’. Proc Natl Acad Sci USA 102:13950–13955PubMedCrossRefGoogle Scholar
  46. Tindall BJ, Rosselló-Móra R, Busse H-J, Ludwig W, Kämpfer P (2010) Notes on the characterisation of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266PubMedCrossRefGoogle Scholar
  47. Trujillo ME (2011) Taxonomic subcommittees and minimal standards for the description of prokaryotes. Microbiology Australia 32:64–66Google Scholar
  48. Turner KME, Feil EJ (2007) The secret life of the multilocus sequence type. Int J Antimicrob Agents 29:129–135PubMedCrossRefGoogle Scholar
  49. Vandamme P, Pot B, Gillis M, de Vos P, Kersters K, Swings J (1996) Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Mol Biol Rev 60:407–438Google Scholar
  50. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Trüper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464CrossRefGoogle Scholar
  51. Woyke T, Tighe D, Mavromatis K, Clum A, Copeland A, Schackwitz W, Lapidus A, Wu D, McCutcheon JP, McDonald BR, Moran NA, Bristow J, Cheng J-F (2010) One bacterial cell, one complete genome. PLOS One 5:e10314PubMedCrossRefGoogle Scholar
  52. Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ, Hooper SD, Pati A, Lykidis A, Spring S, Anderson IJ, D’haeseleer P, Zemla A, Singer M, Lapidus A, Nolan M, Copeland A, Han C, Chen F, Cheng J-F, Lucas S, Kerfeld C, Lang E, Gronow S, Chain P, Bruce D, Rubin EM, Kyrpides NC, Klenk H-P, Eisen JA (2009) A phylogeny-driven genomic encyclopaedia of bacteria and archaea. Nature 462:1056–1060PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Iain C. Sutcliffe
    • 1
  • Martha E. Trujillo
    • 2
  • Michael Goodfellow
    • 3
  1. 1.School of Life SciencesNorthumbria UniversityNewcastle upon TyneUK
  2. 2.Departamento de Microbiología y Genética, Campus Miguel de UnamunoUniversidad de SalamancaSalamancaSpain
  3. 3.School of BiologyUniversity of NewcastleNewcastle upon TyneUK

Personalised recommendations