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Volume 146, Issue 11

High hopanoid/total lipids ratio in mycelia is not related to the nitrogen status Free

Abstract

The GenBank/EMBL/DDBJ accession numbers for the sequences in this paper are AJ251388–91 and AJ251393–4.

Vesicles are specific structures which are produced under nitrogen-limiting culture conditions. Hopanoids are the most abundant lipids in these vesicles and are believed to protect the nitrogenase against oxygen. The amounts and quality of each hopanoid were estimated in different strains cultivated under nitrogen-depleted and nitrogen-replete conditions in order to detect a possible variation. Studied strains nodulating were phylogenetically characterized by analysis of the intergenic region as closely related to genomic species 4 and 5. Phylogenetically different strains belonging to three infectivity groups were cultivated in the same medium with and without nitrogen source for 10 d before hopanoid content analysis by HPLC. Four hopanoids together accounted for 23–87% and 15–87% of the total lipids under nitrogen-replete and nitrogen-depleted culture conditions, respectively. Two of the hopanoids found, bacteriohopanetetrols and their phenylacetic acid esters, have previously been described in . Two new hopanoids, moretan-29-ol and a bacteriohopanetetrol propionate, have also been identified. The moretan-29-ol and bacteriohopanetetrols were found to be the most abundant hopanoids whereas the bacteriohopanetetrol propionate and phenylacetates were present at a concentration close to the limit of detection. The ratio of (bacteriohopanetetrols + moretan-29-ol)/(total lipids) varied in most of the strains between nitrogen-depleted and nitrogen-replete culture conditions. In most of the strains, the hopanoid content was found to be slightly higher under nitrogen-replete conditions than under nitrogen-depleted conditions. These results suggest that remobilization, rather than neosynthesis of hopanoids, is implicated in vesicle formation in under nitrogen-depleted conditions.

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Keyword(s): Frankia strains , hopanoids , lipids and nitrogen
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2000-11-01
2024-12-03
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References

  1. Berry A. M., Torrey J. G. 1979; Isolation and characterisation in vivo and in vitro of an actinomyceteous endophyte from Alnus rubra Bong. In Symbiotic Nitrogen Fixation in the Management of Temperate Forests pp. 69–83Edited by Gordon J. C., Wheeler C. T., Perry D. A. Corvallis: Oregon State University, Forest Research Laboratory;
     [Google Scholar]
  2. Berry A. M., Moreau R. A., Jones A. D. 1991; Bacteriohopanetetrol: abundant lipid in Frankia cells and in nitrogen-fixing nodule tissue. Plant Physiol 95:111–115 [CrossRef]
     [Google Scholar]
  3. Berry A. M., Harriott O. T., Moreau R. A., Osman S. F., Benson D. R., Jones A. D. 1993; Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase. Proc Natl Acad Sci USA 90:6091–6094 [CrossRef]
     [Google Scholar]
  4. Bisseret P., Rohmer M. 1989; Bacterial sterol surrogates. Determination of the absolute configuration of bacteriohopanetetrol side chain by hemisynthesis of its diastereoisomers. J Org Chem 54:2958–2964 [CrossRef]
     [Google Scholar]
  5. Bligh E. G., Dyer W. J. 1959; A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917 [CrossRef]
     [Google Scholar]
  6. Felsenstein J. 1985; Confidence limits on phylogenies: approach using bootstrap. Evolution 39:783–791 [CrossRef]
     [Google Scholar]
  7. Fernandez M. P., Meugnier H., Grimont P. A. D., Bardin R. 1989; Deoxyribonucleic acid relatedness among members of the genus Frankia. Int J Syst Bacteriol 39:424–429 [CrossRef]
     [Google Scholar]
  8. Fontaine M. S., Lancelle S. A., Torrey J. G. 1984; Initiation and ontogeny of vesicles in cultured Frankia sp. strain HFPArI3. J Bacteriol 160:921–927
     [Google Scholar]
  9. Gallon J. R. 1992; Reconciling the incompatible: N2 fixation and O2. New Phytol 122:571–609
     [Google Scholar]
  10. Harriott O. T., Khairallah L., Benson D. R. 1991; Isolation and structure of the lipid envelopes from the nitrogen-fixing vesicles of Frankia sp. strain CpI1. J Bacteriol 173:2061–2067
     [Google Scholar]
  11. Hermans M. A. F., Neuss B., Sahm H. 1991; Content and composition of hopanoids in Zymomonas mobilis under various growth conditions. J Bacteriol 173:5592–5595
     [Google Scholar]
  12. Hirsh A., McKhann H., Reddy A., Liao J., Fang Y., Marshall C. 1995; Assessing horizontal transfer of nif HDK genes in eubacteria: nucleotide sequence of nif K from Frankia strain HFPCcI3. Mol Biol Evol 12:16–27 [CrossRef]
     [Google Scholar]
  13. Jamann S., Fernandez M. P., Normand P. 1993; Typing method for N2-fixing bacteria based on PCR/RFLP application to the characterization of Frankia strains. Mol Ecol 2:17–26 [CrossRef]
     [Google Scholar]
  14. Kannenberg E. L., Perzi M., Muller P., Hartner T., Poralla K. 1996; Hopanoid lipids in Bradyrhizobium and other plant-associated bacteria and cloning of the Bradyrhizobium squalene-hopene cyclase. Plant Soil 186:107–112 [CrossRef]
     [Google Scholar]
  15. Kimura M. 1980; A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120 [CrossRef]
     [Google Scholar]
  16. Kleemann G., Alskog G., Berry A. M., Huss-Danell K. 1994; Lipid composition and nitrogenase activity of the symbiotic Frankia (Alnus incana) in response to different oxygen concentrations. Protoplasma 183:107–115 [CrossRef]
     [Google Scholar]
  17. Lamont L. H., Silvester B., Torrey J. G. 1988; Nile red fluorescence demonstrates lipid in the envelope of vesicles from N2-fixing cultures of Frankia. Can J Microbiol 34:656–660 [CrossRef]
     [Google Scholar]
  18. Marechal J., Clement B., Nalin R., Gandon C., Orso S., Cvejic H., Bruneteau M., Berry A. M., Normand P. 2000; A recA gene analysis confirms the close proximity of Frankia to Acidothermus. Int J Syst Evol Microbiol 50:781–785 [CrossRef]
     [Google Scholar]
  19. Meesters T., van Vliet M., Akkermans A. 1987; Nitrogenase is restricted to the vesicles in Frankia strain EAN1pec. Physiol Plant 70:267–271 [CrossRef]
     [Google Scholar]
  20. Moreau R. A., Asmann P. T., Norman H. A. 1990; Quantitative analysis of the major classes of plant lipids by high performance liquid chromatography and flame ionization detection (HPLC-FID). Phytochemistry 29:2461–2466 [CrossRef]
     [Google Scholar]
  21. Murry M., Fontaine M. S., Torrey J. G. 1984; Growth kinetics and nitrogenase induction in Frankia sp. HFP ArI3 grown in batch culture. Plant Soil 78:61–78 [CrossRef]
     [Google Scholar]
  22. Nalin R., Domenach A. M., Normand P. 1995; Molecular structure of the Frankia spp. nifD-K intergenic spacer and design of Frankia genus compatible primer. Mol Ecol 4:483–491 [CrossRef]
     [Google Scholar]
  23. Nalin R., Normand P., Domenach A. M. 1997; Distribution and N2-fixing activity of Frankia strains in relation with soil depth. Physiol Plant 99:732–738 [CrossRef]
     [Google Scholar]
  24. Nalin R., Normand P., Simonet P., Domenach A. M. 1999; Polymerase chain reaction and hybridization on DNA extracted from soil as a tool for Frankia spp. population distribution studies in soil. Can J Bot 77:1239–1247
     [Google Scholar]
  25. Navarro E., Nalin R., Gauthier D., Normand P. 1997; The nodular microsymbionts of Gymnostoma spp. are Elaeagnus-infective Frankia strains. Appl Environ Microbiol 63:1610–1616
     [Google Scholar]
  26. Oh B., Twiggs P., Hong J., Mullin B., An C. 1997; nif V is contiguous to nif HDK in Frankia strain FaC1. Physiol Plant 99:707–713 [CrossRef]
     [Google Scholar]
  27. Ourisson G., Rohmer M. 1992; The hopanoids. Part 2: the biohopanoids, a novel class of bacterial lipids. Accounts Chem Res 25:403–407 [CrossRef]
     [Google Scholar]
  28. Parsons R., Silvester W., Harris S., Gruijters W., Bullivant S. 1987; Frankia vesicles provide inducible and absolute oxygen protection for nitrogenase. Plant Physiol 83:728–731 [CrossRef]
     [Google Scholar]
  29. Poralla K., Härtner T., Kannenberg E. 1984; Effect of temperature and pH on the hopanoid content of Bacillus acidocaldarius. FEMS Microbiol Lett 23:253–256 [CrossRef]
     [Google Scholar]
  30. Rohmer M. 1993; The biosynthesis of triterpenoids by the hopane series in Eubacteria: a mine of new enzyme reactions. Pure Appl Chem 65:1293–1298
     [Google Scholar]
  31. Rohmer M., Bouvier P., Ourisson G. 1979; Molecular evolution of biomembranes: structural equivalents and phylogenetic precursors of sterols. Proc Natl Acad Sci USA 76:847–851 [CrossRef]
     [Google Scholar]
  32. Rohmer M., Bouvier-Nave P., Ourisson G. 1984; Distribution of hopanoid triterpenes in prokaryotes. J Gen Microbiol 130:1137–1150
     [Google Scholar]
  33. Rosa Putra S. 1998 Ro̧le du 1-désoxy-D-xylulose dans la biosynthèse des isoprénoides PhD thesis Université Louis Pasteur; Strasbourg, France:
     [Google Scholar]
  34. Saitou R. R., Nei M. 1987; A neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
     [Google Scholar]
  35. Schulenberg-Schell H., Neuss B., Sahm H. 1989; Quantitative determination of various hopanoids in microorganisms. Anal Biochem 181:120–124 [CrossRef]
     [Google Scholar]
  36. Shine J., Dalgarno L. 1974; The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementary to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA 71:1342–1346 [CrossRef]
     [Google Scholar]
  37. Silvester W. B., Harris S. L., Tjepkema J. D. 1990; Oxygen regulation and hemoglobin. In The Biology of Frankia and Actinorhizal Plants pp. 157–173Edited by Schwintzer C. R., Tjepkema J. D. New York: Academic Press;
     [Google Scholar]
  38. Simonin P., Jürgens U. J., Rohmer M. 1992; 35–0-β-6-Amino-6-deoxyglucopyranosyl bacteriohopanetetrol, a novel triterpenoid of the hopane series from the cyanobacterium Synechocystis sp. PCC 6714. Tetrahedron Lett 33:3629–3632 [CrossRef]
     [Google Scholar]
  39. Swofford D. L. 1993 paup – phylogenetic analysis using parsimony, version 3.1 Illinois Natural History Survey; Champaign:
     [Google Scholar]
  40. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997; The clustal-x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882 [CrossRef]
     [Google Scholar]
  41. Vilchèze C., Llopiz P., Neunlist S., Poralla K., Rohmer M. 1994; Prokaryotic triterpenoids: new hopanoids from the nitrogen-fixing bacteria Azotobacter vinelandii, Beijerinckia indica and Beijerinckia mobilis. Microbiology 140:2749–2753 [CrossRef]
     [Google Scholar]
  42. Winship P. R. 1989; An improved method for directly sequencing PCR amplified material using dimethyl sulfoxide. Nucleic Acids Res 17:1266 [CrossRef]
     [Google Scholar]
  43. Zhang Z., Torrey J. G. 1985; Studies of an effective strain of Frankia from Allocasuarina lehmanniana of the Casuarinaceae. Plant Soil 87:1–16 [CrossRef]
     [Google Scholar]
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High hopanoid/total lipids ratio in Frankia mycelia is not related to the nitrogen status
Microbiology 146, 3013 (2000); https://doi.org/10.1099/00221287-146-11-3013
/content/journal/micro/10.1099/00221287-146-11-3013
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