Skip to main content
SpringerLink
Log in

The Major Glycerophospholipids of the Predatory and Parasitic Bacterium Bdellovibrio bacteriovorus HID5

  • Original Article
  • Published:
Lipids

Abstract

Bdellovibrio are small motile bacteria that attack and parasitize larger Gram-negative bacteria and since they might have practical applications, these organisms are attracting the attention of researchers as indicated by the sequencing of the B. bacteriovorus genome. There is an earlier report showing that B. bacteriovorus scavenges fatty acids from the host cell during its parasitic phase otherwise the biochemical nature of its lipids, particularly its complex lipids, remains unknown. We here report on the phospholipid classes of an axenically cultured host-independent strain (HID5). Phospholipids and fatty acids were identified by a variety of chromatographic procedures and high-resolution mass spectrometric techniques. Phosphatidylethanolamine was the major phospholipid and phosphatidylserine, cardiolipin, phosphatidylglycerol, and N-acylphosphatidylethanolamine were also identified. The major fatty acids were 16:0, 16:1, 18:1, and 9,10-Mt C16:0 (cyC17:0). Unlike another predatory bacterium, Bacteriovorus stolpii strain UKi2, sphingolipids were not detected in B. bacteriovorus by the procedures used in this study. This is consistent with the apparent lack of genes coding for sphingolipid biosynthesis enzymes in the B. bacteriovorus genome database. The results are consistent with the separation of Bdellovibrio and Bacteriovorus into separate genera.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

AGC:

Automatic gain control

BALO:

Bdellovibrio and like organisms

BHT:

Butylated hydroxytoluene

CL:

Cardiolipin

ddH2O:

Double-distilled water

EI:

Electron ionization

FAME:

Fatty acid methyl esters

FID:

Flame ionization detector

FT-ICR:

Fourier transform-ion cyclotron resonance

HD:

Host-dependent

HID:

Host-independent

GLC:

Gas–liquid chromatograph

HPTLC:

High performance thin-layer chromatography

MS:

Mass spectrometry

NAPE:

N-acylphosphatidylethanolamine

NIST:

National Institute of Standards and Technology

NMR:

Nuclear magnetic resonance

PC:

Phosphatidylcholine

PE:

Phosphatidylethanolamine

PS:

Phosphatidylserine

PG:

Phosphatidylglycerol

MSn :

Tandem mass spectrometry

SPNL:

Sphingophosphonolipids

SIM:

Selective ion monitoring

SS:

Solvent system

TLC:

Thin-layer chromatography

References

  1. Davidov Y, Jurkevitch E (2004) Diversity and evolution of Bdellovibrio-and-like organisms (BALOs), reclassification of Bacteriovorax starrii as Peredibacter starrii gen. nov., comb. nov., and description of the Bacteriovorax-Peredibacter clade as Bacteriovoracaceae fam. nov. Int J Syst Bacteriol 54:1439–1452

    CAS  Google Scholar 

  2. Pineiro SA, Stine OC, Chauhan A, Steyert SR, Smith R, Williams HN (2007) Global survey of diversity among environmental saltwater Bacteriovoracaceae. Environ Microbiol 9:2441–2450

    Article  PubMed  CAS  Google Scholar 

  3. Rendulic S, Jagtap P, Rosinus A, Eppinger M, Baar C, Lanz C, Keller H, Lambert C, Evans KJ, Goesmann A, Meyer F, Sockett RE, Schuster SC (2004) A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 303:689–692

    Article  PubMed  CAS  Google Scholar 

  4. Ruby EG (1981) The genus Bdellovibrio. In: Balows A, Truper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes, 2nd edn. Springer, New York, pp 3400–3415

    Google Scholar 

  5. Starr MP, Baigent NL (1966) Parasitic interaction of Bdellovibrio bacteriovorus with other bacteria. J Bacteriol 91:2006–2017

    PubMed  CAS  Google Scholar 

  6. Stolp H, Starr MP (1963) Bdellovibrio bacteriovorus gen. et sp. n., a predatory ectoparasitic and bacteriolytic microorganism. Antonie van Leeuwenhoek J Microbiol Serol 29:217–248

    Article  CAS  Google Scholar 

  7. Abram D, Castro J, Melo E, Chou D (1974) Penetration of Bdellovibrio bacteriovorus into host cells. J Bacteriol 118:663–680

    PubMed  CAS  Google Scholar 

  8. Evans KJ, Lambert C, Sockett RE (2007) Predation by Bdellovibrio bacteriovorus HD100 requires type IV pili. J Bacteriol 189:4850–4859

    Article  PubMed  CAS  Google Scholar 

  9. Beck S, Schwudke D, Strauch E, Appel B, Linscheid M (2004) Bdellovibrio bacteriovorus strains produce a novel major outer membrane protein during predacious growth in the periplasm of prey bacteria. J Bacteriol 186:2766–2773

    Article  PubMed  CAS  Google Scholar 

  10. Engelking HM, Seidler RJ (1974) The involvement of extracellular enzymes in the metabolism of Bdellovibrio. Arch Mikrobiol 95:293–304

    PubMed  CAS  Google Scholar 

  11. Gray KM, Ruby EG (1990) Prey-derived signals regulating duration of the developmental growth phase of Bdellovibrio bacteriovorus. J Bacteriol 172:4002–4007

    PubMed  CAS  Google Scholar 

  12. Hespell RB (1978) Intraperiplasmic growth of Bdellovibrio bacteriovorus on heat-treated Escherichia coli. J Bacteriol 33:1156–1162

    Google Scholar 

  13. Hespell RB, Miozzari GF, Rittenberg SC (1975) Ribonucleic acid destruction and synthesis during intraperiplasmic growth of Bdellovibrio bacteriovorus. J Bacteriol 123:481–491

    PubMed  CAS  Google Scholar 

  14. Jurkevitch E (2000) The genus Bdellovibrio. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes, Springerg, New York, 33 pp. http://141:150.157.117:8080/prokPUB/index.htm

  15. Kelley JL, Turng BF, Williams HN, Baier M (1997) Effect of temperature, salinity, and substrate on the colonization of surfaces in situ by aquatic bdellovibrios. Appl Environ Microbiol 6:84–90

    Google Scholar 

  16. Sockett RE, Lambert C (2004) Bdellovibrio as therapeutic agents: a predatory renaissance? Nat Rev Microbiol 2:669–675

    Article  PubMed  CAS  Google Scholar 

  17. Wand H, Vacca G, Kuschk P, Krüger M, Kästner M (2007) Removal of bacteria by filtration in planted and non-planted sand columns. Water Res 41:159–167

    Article  PubMed  CAS  Google Scholar 

  18. Yair S, Yaacov D, Susan K, Jurkevitch E (2003) Small eats big: ecology and diversity of Bdellovibrio and like organisms, and their dynamics in predator-prey interactions. Agronomie 23:433–439

    Article  Google Scholar 

  19. Kuenen JG, Rittenberg SC (1975) Incorporation of long-chain fatty acids of the substrate organism by Bdellovibrio bacteriovorax during intraperiplasmic growth. J Bacteriol 121:1145–1157

    PubMed  CAS  Google Scholar 

  20. Nelson DR, Rittenberg SC (1981) Incorporation of substrate cell lipid A components into the lipopolysaccharide of intraperiplasmically grown Bdellovibrio bacteriovorus. J Bacteriol 147:860–868

    PubMed  CAS  Google Scholar 

  21. Nelson DR, Rittenberg SC (1981) Partial characterization of lipid A of intraperiplasmically grown Bdellovibrio bacteriovorus. J Bacteriol 147:869–874

    PubMed  CAS  Google Scholar 

  22. Steiner S, Conti SF, Lester RL (1973) Occurrence of phosphonosphingolipids in Bdellovibrio bacteriovorus strain UKi2. J Bacteriol 116:1199–1211

    PubMed  CAS  Google Scholar 

  23. Baer ML, Ravel J, Chun J, Hill RT, Williams HN (2000) A proposal for the reclassification of Bdellovibrio stolpii and Bdellovibrio starrii into a new genus, Bacteriovorax gen. nov. as Bacteriovorax stolpii comb. nov. and Bacteriovorax starrii comb. nov., respectively. Int J Syst Evol Microbiol 50:219–224

    PubMed  CAS  Google Scholar 

  24. Snyder AR, Williams HN, Baer ML, Walker KE, Stine OC (2002) 16S rDNA sequence analysis of environmental Bdellovibrio-and-like organisms (BALO) reveals extensive diversity. Int J Syst Evol Microbiol 52:2089–2094

    Article  PubMed  CAS  Google Scholar 

  25. Jayasimhulu K, Hunt SM, Watanabe Y, Giner J-L, Kaneshiro ES (2007) Detection and identification of Bacteriovorax stolpii UKi2 sphingophosphonolipid molecular species. J Am Soc Mass Spectrom 18:394–403

    Article  PubMed  CAS  Google Scholar 

  26. Watanabe Y, Nakajima M, Hoshino T, Jayasimhulu K, Brooks EE, Kaneshiro ES (2001) A novel sphingophosphonolipid head group 1-hydroxy-2-aminoethyl phosphonate in Bdellovibrio stolpii. Lipids 36:513–519

    Article  PubMed  CAS  Google Scholar 

  27. Cotter TW, Thomashow MF (1992) Identification of a Bdellovibrio bacteriovorus genetic locus, hit, associated with the host-independent phenotype. J Bacteriol 174:6018–6024

    PubMed  CAS  Google Scholar 

  28. Gordon RF, Stein MA, Diedrich DL (1993) Heat shock-induced axenic growth of Bdellovibrio bacteriovorus. J Bacteriol 175:2157–2161

    PubMed  CAS  Google Scholar 

  29. Ishiguro EE (1973) A growth initiation factor for host-independent derivatives of Bdellovibrio bacteriovorus. J Bacteriol 115:243–252

    PubMed  CAS  Google Scholar 

  30. Seidler RJ, Starr MP (1969) Isolation and characterization of host-independent bdellovibrios. J Bacteriol 100:69–785

    Google Scholar 

  31. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    PubMed  CAS  Google Scholar 

  32. Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    PubMed  CAS  Google Scholar 

  33. Dittmer JC, Lester RL (1964) A simple, specific spray for the detection of phospholipids on thin-layer chromatograms. J Lipid Res 5:126–127

    CAS  Google Scholar 

  34. Kates M (1986) Techniques of lipidology: isolation, analysis and identification of lipids. In: Work TS, Work E (ed), Laboratory techniques in biochemistry and molecular biology, 2nd edn. Elsevier, Amsterdam, pp 220–223

  35. Ferguson KA, Conner RL, Mallory FB, Mallory CW (1972) α-Hydroxy fatty acids in sphingolipids of Tetrahymena. Biochim Biophys Acta 270:111–116

    PubMed  CAS  Google Scholar 

  36. MacGee J, Allen KG (1974) Microanalysis of fatty acids of a small number of whole cells. J Chromatogr 100:35–42

    Article  PubMed  CAS  Google Scholar 

  37. Vincenti M, Guglielmetti G, Cassani G, Tonini C (1987) Determination of double bond position in diunsaturated compounds by mass spectrometry of dimethyl disulfide derivatives. Anal Chem 59:694–699

    Article  Google Scholar 

  38. Pulfer M, Murphy RC (2003) Electrospray mass spectrometry of phospholipids. Mass Spectrom Rev 22:332–364

    Article  PubMed  CAS  Google Scholar 

  39. Cadas H, DiThomaso E, Piomellil D (1997) Occurrence and biosynthesis of endogenous cannabinoid precursor, N-arachidonyl phosphatidylethanolamine, in rat brain. J Neurosci 17:1226–1242

    PubMed  CAS  Google Scholar 

  40. Chapman KD, Moore TS Jr (1993) N-acylphosphatidylethanolamine synthesis in plants: occurrence, molecular composition, and phospholipid origin. Arch Biochem Biophys 301:21–33

    Article  PubMed  CAS  Google Scholar 

  41. Schmid HHO, Schmid PC, Nataranjan V (1990) N-acylated glycerophospholipids and their derivatives. Prog Lipid Res 29:1–43

    Article  PubMed  CAS  Google Scholar 

  42. Ellingson JS (1980) Identification of N-acylethanolamine phosphoglycerides and acylphosphatidylglycerol as the phospholipids which disappeared as Dictyostelium dicoideum cells aggregate. Biochemistry 19:6176–6182

    Article  PubMed  CAS  Google Scholar 

  43. Hazlewood GP, Dawson RMC (1975) Intermolecular transacylation of phosphatidylethanolamine by a Butyrivibrio sp. Biochem J 150:521–525

    PubMed  CAS  Google Scholar 

  44. Kaneshiro ES, Hunt SM, Watanabe Y (2008) Bacteriovorax stolpii proliferation and predation without sphingophosphonolipids. Biochem Biophys Res Commun 367:21–25

    Article  PubMed  CAS  Google Scholar 

  45. Oursel D, Loutelier-Bourhis C, Orange N, Chevalier S, Norris V, Lange CM (2007) Lipid composition of membranes of Escherichia coli by liquid chromatography/tandem mass spectrometry using negative electrospray ionization. Rapid Comm Mass Spectrom 21:1721–1728

    Article  CAS  Google Scholar 

  46. Jurkevitch E, Minz D, Ramati B, Barel G (2000) Prey range characterization, ribotyping, and diversity in soil and rhizosphere Bdellovibrio spp. isolated on phytopathogenic bacteria. Appl Environ Microbiol 66:2365–2371

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Carey Lambert and R. Elizabeth Sockett, Nottingham University for providing cultures of B. bacteriovorus, and Stephen Macha for assistance with mass spectrometer analyses. Supported in part by a grant from the University of Cincinnati Research Council, NIH RO1 AI064084, and NIH RR019900.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, 45221, USA

    Nhu-An T. Nguyen & Edna S. Kaneshiro

  2. Department of Chemistry, University of Cincinnati, Cincinnati, OH, 45221, USA

    Larry Sallans

Authors
  1. Nhu-An T. Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Larry Sallans
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edna S. Kaneshiro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Edna S. Kaneshiro.

About this article

Cite this article

Nguyen, NA.T., Sallans, L. & Kaneshiro, E.S. The Major Glycerophospholipids of the Predatory and Parasitic Bacterium Bdellovibrio bacteriovorus HID5. Lipids 43, 1053–1063 (2008). https://doi.org/10.1007/s11745-008-3235-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-008-3235-9

Keywords

Search

Navigation