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Carl Woese: from Biophysics to Evolutionary Microbiology

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Abstract

This article is a tribute to Carl R. Woese, a biophysicist turned evolutionary microbiologist who passed away on December 30, 2012. We focus on his life, achievements, the discovery of Archaea and contributions to the development of molecular phylogeny. Further, the authors share their views and the lessons learnt from Woese’s life with the microbiologists in India. We also emphasize the need for interdisciplinary collaboration and interaction for the progress and betterment of science.

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References

  1. Alain K, Querellou J (2009) Cultivating the uncultured: limits, advances and future challenges. Extremophiles 13:583–594

    Article  PubMed  Google Scholar 

  2. Brown MV, Schwalbach MS, Hewson I, Fuhrman JA (2005) Coupling 16S-ITS rDNA clone libraries and automated ribosomal intergenic spacer analysis to show marine microbial diversity: development and application to a time series. Environ Microbiol 7:1466–1479

    Article  PubMed  CAS  Google Scholar 

  3. Chauhan NS, Ranjan R, Purohit HJ, Kalia VC, Sharma R (2009) Identification of genes conferring arsenic resistance to Escherichia coli from an effluent treatment plant sludge metagenomic library. FEMS Microbiol Ecol 67:130–139

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  5. Graham DE, Overbeek R, Olsen GJ, Woese CR (2000) An archaeal genomic signature. Proc Natl Acad Sci USA 97:3304–3308

    Article  PubMed  CAS  Google Scholar 

  6. Gupta HK, Gupta RD, Singh A, Chauhan NS, Sharma R (2011) Genome sequence of Rheinheimera sp. strain A13L, isolated from Pangong Lake, India. J Bacteriol 193:5873–5874

    Article  PubMed  CAS  Google Scholar 

  7. Gupta HK, Singh A, Sharma R (2011) Genome sequence of Idiomarina sp. strain A28L, isolated from Pangong Lake, India. J Bacteriol 193:5875–5876

    Article  PubMed  CAS  Google Scholar 

  8. Gupta P, Reddy GSN, Delille D, Shivaji S (2004) Arthrobacter gangotriensis sp. nov. and Arthrobacter kerguelensis sp. nov. from Antarctica. Int J Syst Evol Microbiol 54:2375–2378

    Article  PubMed  CAS  Google Scholar 

  9. Gupta SS, Mohammed MH, Ghosh TS, Kanungo S, Nair GB, Mande SS (2011) Metagenome of the gut of a malnourished child. Gut Pathog 3:7. doi:10.1186/1757-4749-3-7

    Article  PubMed  Google Scholar 

  10. Harris KA, Hartley JC (2003) Development of broad-range 16S rDNA PCR for use in the routine diagnostic clinical microbiology service. J Med Microbiol 52:685–691

    Article  PubMed  CAS  Google Scholar 

  11. Ingham CJ, Sprenkels A, Bomer J, Molenaar D, van den Berg A, van Hylckama Vlieg JE, de Vos WM (2007) The micro-Petri dish, a million-well growth chip for the culture and high-throughput screening of microorganisms. Proc Natl Acad Sci USA 104:18217–18222

    Article  PubMed  CAS  Google Scholar 

  12. Kaeberlein T, Lewis K, Epstein SS (2002) Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296:1227–1229

    Article  Google Scholar 

  13. Kalia VC, Mukherjee T, Bhushan A, Joshi J, Shankar P, Huma N (2011) Analysis of the unexplored features of rrs (16S rDNA) of the genus Clostridium. BMC Genomics 11(12):18. doi:10.1186/1471-2164-12-18

    Article  Google Scholar 

  14. Kostka JE, Prakash O, Overholt W, Green S, Freyer G, Canion A, Delgardio J, Norton N, Huettel M (2011) Hydrocarbon-degrading bacteria and the bacterial community response in Gulf of Mexico beach sands impacted by the Deepwater Horizon oil spill. Appl Environ Microbiol 77:7797–7962

    Article  Google Scholar 

  15. Kuske C, Ticknor LO, Miller ME, Dunbar JM, Davis JA, Barns SM, Belnap J (2002) Comparison of soil bacterial communities in rhizospheres of three plant species and the interspaces in an Arid grassland. Appl Environ Microbiol 68:1854–1863

    Article  PubMed  CAS  Google Scholar 

  16. Lal D, Verma M, Lal R (2011) Exploring internal features of 16S rRNA gene for identification of clinically relevant species of the genus Streptococcus. Ann Clin Microbiol Antimicrob 10:28. doi:10.1186/1476-0711-10-28

    Article  PubMed  CAS  Google Scholar 

  17. Lim J, Do H, Shin SG, Hwang S (2008) Primer and probe sets for group-specific quantification of the genera Nitrosomonas and Nitrosospira using real-time PCR. Biotechnol Bioeng 99:1374–1383

    Article  PubMed  CAS  Google Scholar 

  18. Lu L, Jia Z (2013) Urease gene-containing Archaea dominate autotrophic ammonia oxidation in two acid soils. Environ Microbiol. doi:10.1111/1462-2920.12071

    Google Scholar 

  19. Macrae A (2000) The use of 16S rDNA methods in soil microbial ecology. Brazil J Microbiol 31:77–82

    Article  CAS  Google Scholar 

  20. Marathe N, Shetty S, Lanjekar V, Ranade D, Shouche Y (2012) Changes in human gut flora with age: an Indian familial study. BMC Microbiol 12:222. doi:10.1186/1471-2180-12-222

    Article  PubMed  Google Scholar 

  21. Morell V (1997) Microbial biology: microbiology’s scarred revolutionary. Science 276:699–702. doi:10.1126/science.276.5313.699

    Article  PubMed  CAS  Google Scholar 

  22. Olsen GJ, Woese CR (1993) Ribosomal RNA: a key to phylogeny. FASEB J 7:113–123

    PubMed  CAS  Google Scholar 

  23. Olsen GJ, Woese CR, Overbeek R (1994) The winds of (evolutionary) change: breathing new life into microbiology. J Bacteriol 176:1–6

    PubMed  CAS  Google Scholar 

  24. Pace NR, Stahl DA, Lane DJ, Olsen GJ (1986) The analysis of natural microbial populations by ribosomal RNA sequences. Adv Microb Ecol 9:1–55

    CAS  Google Scholar 

  25. Pandey PK, Siddharth J, Verma P, Bavdekar A, Patole MS, Shouche YS (2012) Molecular typing of fecal eukaryotic microbiota of human infants and their respective mothers. J Biosci 37:221–226

    Article  PubMed  Google Scholar 

  26. Patil DP, Dhotre DP, Chavan SG, Sultan A, Jain DS, Lanjekar VB, Gangawani J, Shah PS, Todkar JS, Shah S, Ranade DR, Patole MS, Shouche YS (2012) Molecular analysis of gut microbiota in obesity among Indian individuals. J Biosci 37:647–657

    Article  PubMed  CAS  Google Scholar 

  27. Pereira E, Silva MC, Dias AC, van Elsas JD, Salles JF (2012) Spatial and temporal variation of archaeal, bacterial and fungal communities in agricultural soils. PLoS ONE 7(12):e51554

    Article  Google Scholar 

  28. Porwal S, Lal S, Cheema S, Kalia VC (2009) Phylogeny in aid of the present and novel microbial lineages: diversity in Bacillus. PLoS ONE 4(2):e4438. doi:10.1371/journal.pone.0004438

    Article  PubMed  Google Scholar 

  29. Prakash O, Lal R (2006) Description of Sphingobium fuliginis sp. nov., a phenanthrene degrading bacterium from fly ash dumping site, and reclassification of Sphingomonas cloacae as Sphingobium cloacae comb. nov. Int J Syst Evol Microbiol 56:2147–2152

    Article  PubMed  CAS  Google Scholar 

  30. Prakash O, Kumari K, Lal R (2007) Pseudomonas delhiensis sp. nov, from a fly ash dumping site of a thermal power plant. Int J Syst Evol Microbiol 57:527–531

    Article  PubMed  CAS  Google Scholar 

  31. Prakash O, Nimonkar Y, Shouche YS (2013) Practice and prospects of microbial preservation. FEMS Microbiol Lett 339:1–9

    Article  PubMed  CAS  Google Scholar 

  32. Prakash O, Shouche Y, Jangid K, Kostka JE (2013) Microbial cultivation and the role of microbial resource centers in the omics era. Appl Microbiol Biotechnol 97:51–62. doi:10.1007/s00253-012-4533-y

    Article  PubMed  CAS  Google Scholar 

  33. Purohit HJ, Raje DV, Kapley A (2007) Identification of signature and primers specific to genus Pseudomonas using mismatched patterns of 16S rDNA sequences. BMC Bioinform 4(1):19

    Article  Google Scholar 

  34. Raina V, Suar M, Singh A, Prakash O, Dadhwal M, Gupta SK, Lal R (2008) Enhanced biodegradation of hexachlorocyclohexane (HCH) in contaminated soils via inoculation with Sphingobium indicum B90A. Biodegradation 19:27–40

    Article  PubMed  CAS  Google Scholar 

  35. Rani A, Porwal S, Sharma R, Kapley A, Purohit HJ, Kalia VC (2008) Assessment of microbial diversity in effluent treatment plants by culture dependent and culture independent approaches. Bioresour Technol 99:7098–7107

    Article  PubMed  CAS  Google Scholar 

  36. Rappé MS, Connon SA, Vergin KL, Giovannoni SJ (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418:630–633

    Article  PubMed  Google Scholar 

  37. Reddy GSN, Uttam A, Shivaji S (2008) Bacillus cecembensis sp. nov., isolated from the Pindari glacier of the Indian Himalayas. Int J Syst Evol Microbiol 58:2330–2335

    Article  PubMed  CAS  Google Scholar 

  38. Roberts E, Sethi A, Montoya J, Woese CR, Luthey-Schulten Z (2008) Molecular signatures of ribosomal evolution. Proc Natl Acad Sci USA 105:13953–13958

    Article  PubMed  CAS  Google Scholar 

  39. Sangwan N, Lata P, Dwivedi V, Singh A, Niharika N, Kaur J, Anand S, Malhotra J, Jindal S, Nigam A, Lal D, Dua A, Saxena A, Garg N, Verma M, Kaur J, Mukherjee U, Gilbert JA, Dowd SE, Raman R, Khurana P, Khurana JP, Lal R (2012) Comparative metagenomic analysis of soil microbial communities across three hexachlorocyclohexane contamination levels. PLoS ONE 7(9):e46219. doi:10.1371/journal.pone.0046219

    Article  PubMed  CAS  Google Scholar 

  40. Schütte UM, Abdo Z, Bent SJ, Shyu C, Williams CJ, Pierson JD, Forney LJ (2008) Advances in the use of terminal restriction fragment length polymorphism (T-RFLP) analysis of 16S rRNA genes to characterize microbial communities. Appl Microbiol Biotechnol 80:365–380

    Article  PubMed  Google Scholar 

  41. Selvakumaran S, Kapley A, Kalia VC, Purohit HJ (2011) Phenotypic and phylogenic groups to evaluate the diversity of Citrobacter isolates from activated biomass of effluent treatment plants. Bioresour Technol 102:4600–4609. doi:10.1016/j.biortech.2011.01.011

    Article  PubMed  CAS  Google Scholar 

  42. Srinivas TNR, Rao S, Reddy PVV, Pratibha MS, Sailaja B, Kavya B, Hara Kishore K, Begum Z, Singh SM, Shivaji S (2009) Bacterial diversity and bioprospecting for cold-active lipases, amylases and proteases, from culturable bacteria of Kongsfjorden and Ny-Alesund, Svalbard, Arctic. Curr Microbiol 59:537–547

    Article  PubMed  CAS  Google Scholar 

  43. Sundarakrishnan B, Pushpanathan M, Jayashree S, Rajendhran J, Sakthivel N, Jayachandran S, Gunasekaran P (2012) Assessment of microbial richness in pelagic sediment of Andaman sea by bacterial tag encoded FLX titanium amplicon pyrosequencing (bTEFAP). Ind J Microbiol 52:544–550

    Article  CAS  Google Scholar 

  44. Tomohiro T, Futoshi K, Ikuro K, Hiroaki F (2011) Shotgun isotope array for rapid, substrate-specific detection of microorganisms in a microbial community. Appl Environ Microbiol 77:7430–7432

    Article  Google Scholar 

  45. Vidya J, Swaroop S, Singh SK, Alex D, Sukumaran RK, Pandey A (2011) Isolation and characterization of a novel α-amylase from a metagenomic library of Western Ghats of Kerala, India. Biologia 66:939–944

    Article  CAS  Google Scholar 

  46. Wheelis ML, Kandler O, Woese CR (1992) On the nature of global classification. Proc Natl Acad Sci USA 89:2930–2934

    Article  PubMed  CAS  Google Scholar 

  47. Woese CR, John RF (1960) Correlations between ribonucleic acid and deoxyribonucleic acid metabolism during spore germination. J Bacteriol 80:811

    PubMed  CAS  Google Scholar 

  48. Woese CR (1958) Comparison of the X-ray sensitivity of bacterial spores. J Bacteriol 75:5–8

    PubMed  CAS  Google Scholar 

  49. Woese CR (1965) On the evolution of the genetic code. Proc Natl Acad Sci USA 54:1546–1552

    Article  PubMed  CAS  Google Scholar 

  50. Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    PubMed  CAS  Google Scholar 

  51. Woese CR (1994) Microbiology in transition. Proc Natl Acad Sci USA 91:1601–1603

    Article  PubMed  CAS  Google Scholar 

  52. Woese CR (1994) There must be a prokaryote somewhere: microbiology’s search for itself. Microbiol Rev 58:1–9

    PubMed  CAS  Google Scholar 

  53. Woese CR (2000) Interpreting the universal phylogenetic tree. Proc Natl Acad Sci USA 97:8392–8396

    Article  PubMed  CAS  Google Scholar 

  54. Woese CR (2002) On the evolution of cells. Proc Natl Acad Sci USA 99:8742–8747

    Article  PubMed  CAS  Google Scholar 

  55. Woese CR (2004) A new biology for a new century. Microbiol Mol Biol Rev 68:173–186

    Article  PubMed  CAS  Google Scholar 

  56. Woese CR (2006) How we do, don’t and should look at bacteria and bacteriology. Prokaryotes 1:3–23

    Article  Google Scholar 

  57. Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090

    Article  PubMed  CAS  Google Scholar 

  58. Woese CR, Kandler O, Wheelies Wheelies ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:457

    Google Scholar 

  59. Zengler K, Toledo C, Rappe M, Elkins J, Mathur EJ, Short JM, Keller M (2002) Cultivating the uncultured. Proc Natl Acad Sci USA 99:15681–15686

    Article  PubMed  CAS  Google Scholar 

  60. Zuckerkandl E, Pauling L (1965) Molecules as documents of evolutionary history. J Theor Biol 8:357–366

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Department of Biotechnology (DBT; Grant no. BT/PR/0054/NDB/52/94/2007), Government of India, under the project “Establishment of microbial culture collection”. We are grateful to our colleagues, especially Shreyas Kumbhare and Somak Chowdhury, for critically reading and editing the manuscript.

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  1. Microbial Culture Collection, National Centre for Cell Science, Ganeshkhind, Pune, 411007, Maharashtra, India

    Om Prakash, Kamlesh Jangid & Yogesh S. Shouche

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  1. Om Prakash
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  2. Kamlesh Jangid
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  3. Yogesh S. Shouche
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Correspondence to Yogesh S. Shouche.

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Prakash, O., Jangid, K. & Shouche, Y.S. Carl Woese: from Biophysics to Evolutionary Microbiology. Indian J Microbiol 53, 247–252 (2013). https://doi.org/10.1007/s12088-013-0401-4

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