Advertisement

Microbial Ecology

, Volume 48, Issue 1, pp 120–127 | Cite as

Micrococcus luteus - Survival in Amber

  • C.L. Greenblatt
  • J. Baum
  • B.Y. Klein
  • S. Nachshon
  • V. Koltunov
  • R.J. Cano
Article

Abstract

A growing body of evidence now supports the isolation of microorganisms from ancient materials. However, questions about the stringency of extraction methods and the genetic relatedness of isolated organisms to their closest living relatives continue to challenge the authenticity of these ancient life forms. Previous studies have successfully isolated a number of spore-forming bacteria from organic and inorganic deposits of considerable age whose survival is explained by their ability to enter suspended animation for extended periods of time. However, despite a number of putative reports, the isolation of non-spore-forming bacteria and an explanation for their survival have remained enigmatic. Here we describe the isolation of non-spore-forming cocci from a 120-million-year-old block of amber, which by genetic, morphological, and biochemical analyses are identified as belonging to the bacterial species Micrococcus luteus. Although comparison of 16S rRNA sequences from the ancient isolates with their modern counterparts is unable to confirm the precise age of these bacteria, we demonstrate, using complementary molecular and cell biological techniques, evidence supporting the view that these (and related modern members of the genus) have numerous adaptations for survival in extreme, nutrient-poor environments, traits that will assist in this bacteria’s persistence and dispersal in the environment. The bacteria’s ability to utilize succinic acid and process terpine-related compounds, both major components of natural amber, support its survival in this oligotrophic environment.

Keywords

Succinic Acid Minimum Bactericidal Concentration Micrococcus Luteus Minimum Bactericidal Concentration Tuberculostearic Acid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We are grateful to the Center for the Study of Emerging Diseases for their generous support. Professor A. Nissenbaum from the Weizmann Institute of Science kindly provided the samples of amber used in the study.

References

  1. 1.
    Bamji, MS, Krinsky, NI 1966The carotenoid pigments of a radiation-resistant Micrococcus species.Biochim Biophys Acta115276284CrossRefPubMedGoogle Scholar
  2. 2.
    Budavari, S 1989The Merck IndexMerck & CoRahway, NJGoogle Scholar
  3. 3.
    Cano, RJ, Borucki, MK 1995Revival and identification of bacterial spores in 25- to 40-million-year-old Dominican amber.Science26810601064PubMedGoogle Scholar
  4. 4.
    Carson, CF, Riley, TV (1998) Antimicrobial activity of tea tree oil—a report for the Rural Industries Research and Development Corporation (Australia). RIRDC Publication number 98/70, pp 1–52 (http://wwwrirdcgovau/reports/TTO/UWA-24Adoc)
  5. 5.
    Crowe, BA, Owen, P 1983Molecular properties of succinate dehydrogenase isolated from Micrococcus luteus (lysodeikticus).J Bacteriol15314931501PubMedGoogle Scholar
  6. 6.
    Czapek, F 1922Biochemie der Pflanzen, 3FischerJenaGoogle Scholar
  7. 7.
    Davey, HM, Kaprelyants, AS, Kell, DB 1993Flow cytometric analysis, using rhodamine 123, of Micrococcus luteus at low growth rate in chemostat culture.Lloyd, D eds. Flow Cytometry in MicrobiologySpringer-VerlagLondon8393Google Scholar
  8. 8.
    Galippe, V 1920Recherches sur la resistence de microzymes a l’ action du temps et sur leur survivance dans l’amber.Compt Rend Acad Sci (Paris)170856858Google Scholar
  9. 9.
    Graur, D, Pupko, T 2001The Permian bacterium that isn’t.Mol Biol Evol1811431146PubMedGoogle Scholar
  10. 10.
    Greenblatt, CL, Davis, A, Clement, BG, Kitts, CL, Cox, T, Cano, RJ 1999Diversity of microorganisms isolated from amber.Microb Ecol385868CrossRefPubMedGoogle Scholar
  11. 11.
    Hopfenberg, HB, Witchey, LC, Poinar, GO, Beck, CW, Chave, KE, Smith, SV, Horibe, Y 1988Is the air in amber ancient?; discussions and reply.Science241717724Google Scholar
  12. 12.
    Imshenetsky, AA, Lysenko, SV, Lach, SP 1979Microorganisms of the upper layer of the atmosphere and the protective role of their cell pigments.Life Sci Space Res17105110PubMedGoogle Scholar
  13. 13.
    Kaprelyants, AS, Kell, DB 1992Rapid assessment of bacterial viability and vitality using rhodamine 123 and flow cytometry.J Appl Bacteriol72410422Google Scholar
  14. 14.
    Kaprelyants, AS, Kell, DB 1993Dormancy in stationary-phase cultures of Micrococcus luteus: flow cytometric analysis of starvation and resuscitation.Appl Environ Microbiol5931873196Google Scholar
  15. 15.
    Kennedy, MJ, Reader, SL, Swierczynski, LM 1994Preservation records of microorganisms: evidence of the tenacity of life.Microbiology14025132529PubMedGoogle Scholar
  16. 16.
    Lambert, JB, Frye, JS 1982Carbon functionalities in amber.Science2175557Google Scholar
  17. 17.
    Lambert, LH, Cox, T, Mitchell, K, Rossello-Mora, RA, Del Cueto, C, Dodge, DE, Orkand, P, Cano, RJ 1998 Staphylococcus succinus sp nov, isolated from Dominican amber.Int J Syst Bacteriol48511518PubMedGoogle Scholar
  18. 18.
    Lancaster, CR 2002Succinate:quinone oxidoreductases: an overview.Biochim Biophys Acta155316CrossRefPubMedGoogle Scholar
  19. 19.
    Madigan, MT, Martinko, JM, Parker, J 2000Brock: Biology of Microorganisms, 9Prentice HallUpper Saddle River, NJGoogle Scholar
  20. 20.
    Mathews, MM, Krinsky, NI 1965The relationship between carotenoid pigments and resistance to radiation in non-photosynthetic bacteria.Photochem Photobiol4813817PubMedGoogle Scholar
  21. 21.
    Mattimore, V, Battista, JR 1996Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation.J Bacteriol178633637PubMedGoogle Scholar
  22. 22.
    Maughan, H, Birky Jr, CW, Nicholson, WL, Rosenzweig, WD, Vreeland, RH 2002The paradox of the “ancient” bacterium which contains “modern” protein-coding genes.Mol Biol Evol1916371639PubMedGoogle Scholar
  23. 23.
    Minton, KW, Daly, MJ 1995A model for repair of radiation-induced DNA double-strand breaks in the extreme radiophile Deinococcus radiodurans.Bioessays17457464PubMedGoogle Scholar
  24. 24.
    Morita, RY 1999Is H2 the universal energy source for long-term survival?Microb Ecol38307320CrossRefPubMedGoogle Scholar
  25. 25.
    Mukamolova, GV, Kaprelyants, AS, Young, DI, Young, M, Kell, DB 1998A bacterial cytokine.Proc Natl Acad Sci USA9589168921CrossRefPubMedGoogle Scholar
  26. 26.
    Mukamolova, GV, Kormer, SS, Kell, DB, Kaprelyants, AS 1999Stimulation of the multiplication of Micrococcus luteus by an autocrine growth factor.Arch Microbiol172914CrossRefPubMedGoogle Scholar
  27. 27.
    Nicholson, WL, Munakata, N, Horneck, G, Melosh, HJ, Setlow, P 2000Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments.Microbiol Mol Biol Rev64548572Google Scholar
  28. 28.
    Nickle, DC, Learn, GH, Rain, MW, Mullins, JI, Mittler, JE 2002Curiously modern DNA for a “250 million-year-old” bacterium.J Mol Evol54134137PubMedGoogle Scholar
  29. 29.
    Nissenbaum, A 1975Lower Cretaceous amber from Israel.Naturwissenschaften62341342Google Scholar
  30. 30.
    Oh, SK, Han, KH, Ryu, SB, Kang, H 2000Molecular cloning, expression, and functional analysis of a cis-prenyltransferase from Arabidopsis thaliana. Implications in rubber biosynthesis.J Biol Chem2751848218488CrossRefPubMedGoogle Scholar
  31. 31.
    Poinar, GO, Poinar, R 1994The Quest for Life in AmberAddison-WesleyNew YorkGoogle Scholar
  32. 32.
    Saito, Y, Ogura, K 1981Biosynthesis of menaquinones Enzymatic prenylation of 1,4-dihydroxy-2-naphthoate by Micrococcus luteus membrane fractions.J Biochem (Tokyo)8914451452Google Scholar
  33. 33.
    Salton, MR, Schmitt, MD 1967Effects of diphenylamine on carotenoids and menaquinones in bacterial membranes.Biochim Biophys Acta135196207CrossRefPubMedGoogle Scholar
  34. 34.
    Shimizu, N, Koyama, T, Ogura, K 1998Molecular cloning, expression, and purification of undecaprenyl diphosphate synthase No sequence similarity between E- and Z-prenyl diphosphate synthases.J Biol Chem2731947619481CrossRefPubMedGoogle Scholar
  35. 35.
    Stackebrandt, E, Goebel, BM 1994Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology.Int J Syst Bacteriol44846849Google Scholar
  36. 36.
    Tanaka, T, Burgess, JG, Wright, PC 2001High-pressure adaptation by salt stress in a moderately halophilic bacterium obtained from open seawater.Appl Microbiol Biotechnol57200204CrossRefPubMedGoogle Scholar
  37. 37.
    Vreeland, RH, Rosenzweig, WD, Powers, DW 2000Isolation of a 250 million-year-old halotolerant bacterium from a primary salt crystal.Nature407897900CrossRefPubMedGoogle Scholar
  38. 38.
    Warringa, MG, Giuditta, A 1958Studies on succinic dehydrogenase. IX. Characterisation of the enzyme from Micrococcus lactilyticus.J Biol Chem230111123PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • C.L. Greenblatt
    • 1
  • J. Baum
    • 1
  • B.Y. Klein
    • 1
  • S. Nachshon
    • 1
  • V. Koltunov
    • 1
  • R.J. Cano
    • 2
  1. 1.Kuvin Centre for the Study of Infectious and Tropical DiseaseThe Hebrew University—Hadassah School of MedicineJerusalemIsrael
  2. 2.Biological Sciences DepartmentCalifornia Polytechnic State UniversitySan Luis ObispoUSA

Personalised recommendations