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. 1994 Jan;60(1):120–125. doi: 10.1128/aem.60.1.120-125.1994

Phase Variation in Xenorhabdus nematophilus and Photorhabdus luminescens: Differences in Respiratory Activity and Membrane Energization

Adam J Smigielski 1,*, Raymond J Akhurst 1, Noël E Boemare 1,
PMCID: PMC201278  PMID: 16349145

Abstract

Phase variation in Xenorhabdus and Photorhabdus spp. has a significant impact on their symbiotic relationship with entomopathogenic nematodes by altering the metabolic by-products upon which the nematodes feed. The preferential retention of the phase I variant by the infective-stage nematode and its better support for nematode reproduction than phase II indicates its importance in the bacterial-nematode interactions. However, there is no obvious role for phase II in these interactions. This study has revealed differences in the respiratory activity between the two phases of Xenorhabdus nematophilus A24 and Photorhabdus luminescens Hm. After experiencing periods of starvation, phase II cells recommenced growth within 2 to 4 h from the addition of nutrients, compared with 14 h for phase I cells, indicating a more efficient nutrient uptake ability in the former. The levels of activity of major respiratory enzymes were 15 to 100% higher in phase II cells from stationary cultures in complex media than in phase I cells. Transmembrane proton motive force measurements were also higher by 20% in phase II under the same conditions. The increased membrane potentials reflect upon the ability of the phase II variant to respond to nutrients, both through growth and nutrient uptake. It is postulated that while phase I cells are better adapted to conditions in the insect and the nematode, phase II cells may be better adapted to conditions in soil as free-living organisms.

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Selected References

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  1. Akhurst R. J. Antibiotic activity of Xenorhabdus spp., bacteria symbiotically associated with insect pathogenic nematodes of the families Heterorhabditidae and Steinernematidae. J Gen Microbiol. 1982 Dec;128(12):3061–3065. doi: 10.1099/00221287-128-12-3061. [DOI] [PubMed] [Google Scholar]
  2. Akhurst R. J., Boemare N. E. A numerical taxonomic study of the genus Xenorhabdus (Enterobacteriaceae) and proposed elevation of the subspecies of X. nematophilus to species. J Gen Microbiol. 1988 Jul;134(7):1835–1845. doi: 10.1099/00221287-134-7-1835. [DOI] [PubMed] [Google Scholar]
  3. Bragg P. D., Hou C. Reduced nicotinamide adenine dinucleotide oxidation in Escherichia coli particles. I. Properties and cleavage of the electron transport chain. Arch Biochem Biophys. 1967 Mar;119(1):194–201. doi: 10.1016/0003-9861(67)90446-8. [DOI] [PubMed] [Google Scholar]
  4. Bryan L. E., Van Den Elzen H. M. Effects of membrane-energy mutations and cations on streptomycin and gentamicin accumulation by bacteria: a model for entry of streptomycin and gentamicin in susceptible and resistant bacteria. Antimicrob Agents Chemother. 1977 Aug;12(2):163–177. doi: 10.1128/aac.12.2.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Butlin J. D., Cox G. B., Gibson F. Oxidative phosphorylation in Escherichia coli K-12: the genetic and biochemical characterisations of a strain carrying a mutation in the uncB gene. Biochim Biophys Acta. 1973 Feb 22;292(2):366–375. doi: 10.1016/0005-2728(73)90043-1. [DOI] [PubMed] [Google Scholar]
  6. Chappell J. B. The oxidation of citrate, isocitrate and cis-aconitate by isolated mitochondria. Biochem J. 1964 Feb;90(2):225–237. doi: 10.1042/bj0900225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. DAVIS B. D., MINGIOLI E. S. Mutants of Escherichia coli requiring methionine or vitamin B12. J Bacteriol. 1950 Jul;60(1):17–28. doi: 10.1128/jb.60.1.17-28.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Feldmann K. New devices for flow dialysis and ultrafiltration for the study of protein--ligand interactions. Anal Biochem. 1978 Jul 15;88(1):225–235. doi: 10.1016/0003-2697(78)90414-1. [DOI] [PubMed] [Google Scholar]
  9. Haddock B. A., Jones C. W. Bacterial respiration. Bacteriol Rev. 1977 Mar;41(1):47–99. doi: 10.1128/br.41.1.47-99.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Herbert A. A., Guest J. R. Two mutations affecting utilization of C4-dicarboxylic acids by Escherichia coli. J Gen Microbiol. 1970 Oct;63(2):151–162. doi: 10.1099/00221287-63-2-151. [DOI] [PubMed] [Google Scholar]
  11. King E. J. The colorimetric determination of phosphorus. Biochem J. 1932;26(2):292–297. doi: 10.1042/bj0260292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  13. Poinar G. O., Jr, Thomas G. M. Significance of Achromobacter nematophilus Poinar and Thomas (Achromobacteraceae: Eubacteriales) in the development of the nematode, DD-136 (Neoaplectana sp. Steinernematidae). Parasitology. 1966 May;56(2):385–390. doi: 10.1017/s0031182000070980. [DOI] [PubMed] [Google Scholar]
  14. Rottenberg H. The measurement of membrane potential and deltapH in cells, organelles, and vesicles. Methods Enzymol. 1979;55:547–569. doi: 10.1016/0076-6879(79)55066-6. [DOI] [PubMed] [Google Scholar]
  15. Schuldiner S., Rottenberg H., Avron M. Determination of pH in chloroplasts. 2. Fluorescent amines as a probe for the determination of pH in chloroplasts. Eur J Biochem. 1972 Jan 31;25(1):64–70. doi: 10.1111/j.1432-1033.1972.tb01667.x. [DOI] [PubMed] [Google Scholar]
  16. Taylor B. L. Role of proton motive force in sensory transduction in bacteria. Annu Rev Microbiol. 1983;37:551–573. doi: 10.1146/annurev.mi.37.100183.003003. [DOI] [PubMed] [Google Scholar]
  17. Wallace B. J., Young I. G. Role of quinones in electron transport to oxygen and nitrate in Escherichia coli. Studies with a ubiA- menA- double quinone mutant. Biochim Biophys Acta. 1977 Jul 7;461(1):84–100. doi: 10.1016/0005-2728(77)90071-8. [DOI] [PubMed] [Google Scholar]

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