1887

Abstract

The contribution of N-acetylneuraminate scavenging to the nutrition of Mycoplasma alligatoris was examined. The wild-type grew substantially faster (P<0.01) than the mutant strains that were unable either to liberate (extracellular NanI mutants) or to catabolize (NanA mutants) N-acetylneuraminate from glycoconjugates in minimal SP-4 medium supplemented only with serum, but the growth of sialidase-negative mutants could not be restored to wild-type rate simply by adding unconjugated sialic acid to the culture medium. In 1 : 1 growth competition assays the wild-type was recovered in >99-fold excess of a sialidase-negative mutant after co-culture on pulmonary fibroblasts in serum-free RPMI 1640 medium, even with supplemental glucose. The advantage of nutrient scavenging via this mechanism in a complex glycan-rich environment may help to balance the expected selective disadvantage conferred by the pathogenic effects of mycoplasmal sialidase in an infected host.

Keyword(s): growth , Mycoplasma , nutrition and sialidase
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/content/journal/micro/10.1099/mic.0.000739
2018-11-13
2019-09-24
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References

  1. Almagro-Moreno S, Boyd EF. Insights into the evolution of sialic acid catabolism among bacteria. BMC Evol Biol 2009;9:118 [CrossRef][PubMed]
    [Google Scholar]
  2. Almagro-Moreno S, Boyd EF. Bacterial catabolism of nonulosonic (sialic) acid and fitness in the gut. Gut Microbes 2010;1:45–50 [CrossRef][PubMed]
    [Google Scholar]
  3. Vimr ER. Unified theory of bacterial sialometabolism: how and why bacteria metabolize host sialic acids. ISRN Microbiol 2013;2013:1–26 [CrossRef][PubMed]
    [Google Scholar]
  4. Vimr ER, Troy FA. Identification of an inducible catabolic system for sialic acids (nan) in Escherichia coli. J Bacteriol 1985;164:845–853[PubMed]
    [Google Scholar]
  5. Honma K, Ruscitto A, Frey AM, Stafford GP, Sharma A. Sialic acid transporter NanT participates in Tannerella forsythia biofilm formation and survival on epithelial cells. Microb Pathog 2016;94:12–20 [CrossRef][PubMed]
    [Google Scholar]
  6. Li J, McClane BA. NanI sialidase can support the growth and survival of Clostridium perfringens strain F4969 in the presence of sialyated host macromolecules (Mucin) or Caco-2 cells. Infect Immun 2018;86:e00547-17 [CrossRef][PubMed]
    [Google Scholar]
  7. Mally M, Shin H, Paroz C, Landmann R, Cornelis GR. Capnocytophaga canimorsus: a human pathogen feeding at the surface of epithelial cells and phagocytes. PLoS Pathog 2008;4:e1000164 [CrossRef][PubMed]
    [Google Scholar]
  8. Roy S, Honma K, Douglas CW, Sharma A, Stafford GP. Role of sialidase in glycoprotein utilization by Tannerella forsythia. Microbiology 2011;157:3195–3202 [CrossRef][PubMed]
    [Google Scholar]
  9. Vimr ER, Kalivoda KA, Deszo EL, Steenbergen SM. Diversity of microbial sialic acid metabolism. Microbiol Mol Biol Rev 2004;68:132–153 [CrossRef][PubMed]
    [Google Scholar]
  10. Brown DR, Farmerie WG, May M, Benders GA, Durkin AS et al. Genome sequences of Mycoplasma alligatoris A21JP2T and Mycoplasma crocodyli MP145T. J Bacteriol 2011;193:2892–2893 [CrossRef][PubMed]
    [Google Scholar]
  11. Brown DR, Zacher LA, Farmerie WG. Spreading factors of Mycoplasma alligatoris, a flesh-eating mycoplasma. J Bacteriol 2004;186:3922–3927 [CrossRef][PubMed]
    [Google Scholar]
  12. Hunt ME, Brown DR. Mycoplasma alligatoris infection promotes CD95 (FasR) expression and apoptosis of primary cardiac fibroblasts. Clin Diagn Lab Immunol 2005;12:1370–1377 [CrossRef][PubMed]
    [Google Scholar]
  13. Hunt ME, Brown DR. Role of sialidase in Mycoplasma alligatoris-induced pulmonary fibroblast apoptosis. Vet Microbiol 2007;121:73–82 [CrossRef][PubMed]
    [Google Scholar]
  14. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004;340:783–795 [CrossRef][PubMed]
    [Google Scholar]
  15. Severi E, Hood DW, Thomas GH. Sialic acid utilization by bacterial pathogens. Microbiology 2007;153:2817–2822 [CrossRef][PubMed]
    [Google Scholar]
  16. Severi E, Hosie AH, Hawkhead JA, Thomas GH. Characterization of a novel sialic acid transporter of the sodium solute symporter (SSS) family and in vivo comparison with known bacterial sialic acid transporters. FEMS Microbiol Lett 2010;304:47–54 [CrossRef][PubMed]
    [Google Scholar]
  17. Teplyakov A, Obmolova G, Toedt J, Galperin MY, Gilliland GL. Crystal structure of the bacterial YhcH protein indicates a role in sialic acid catabolism. J Bacteriol 2005;187:5520–5527 [CrossRef][PubMed]
    [Google Scholar]
  18. Jaeger T, Mayer C. N-acetylmuramic acid 6-phosphate lyases (MurNAc etherases): role in cell wall metabolism, distribution, structure, and mechanism. Cell Mol Life Sci 2008;65:928–939 [CrossRef][PubMed]
    [Google Scholar]
  19. Corfield T. Bacterial sialidases–roles in pathogenicity and nutrition. Glycobiology 1992;2:509–521 [CrossRef][PubMed]
    [Google Scholar]
  20. Schauer R. Achievements and challenges of sialic acid research. Glycoconj J 2000;17:485–499 [CrossRef][PubMed]
    [Google Scholar]
  21. Dybvig K, Zuhua C, Lao P, Jordan DS, French CT et al. Genome of Mycoplasma arthritidis. Infect Immun 2008;76:4000–4008 [CrossRef][PubMed]
    [Google Scholar]
  22. May M, Brown DR. Secreted sialidase activity of canine mycoplasmas. Vet Microbiol 2009;137:380–383 [CrossRef][PubMed]
    [Google Scholar]
  23. Løbner-Olesen A, Skovgaard O, Marinus MG. Dam methylation: coordinating cellular processes. Curr Opin Microbiol 2005;8:154–160 [CrossRef][PubMed]
    [Google Scholar]
  24. Jeong HG, Oh MH, Kim BS, Lee MY, Han HJ et al. The capability of catabolic utilization of N-acetylneuraminic acid, a sialic acid, is essential for Vibrio vulnificus pathogenesis. Infect Immun 2009;77:3209–3217 [CrossRef][PubMed]
    [Google Scholar]
  25. Corfield AP, Higa H, Paulson JC, Schauer R. The specificity of viral and bacterial sialidases for alpha(2-3)- and alpha(2-6)-linked sialic acids in glycoproteins. Biochim Biophys Acta 1983;744:121–126 [CrossRef][PubMed]
    [Google Scholar]
  26. Sethi KK, Müller HE. Neuraminidase activity in Mycoplasma gallisepticum. Infect Immun 1972;5:260–262[PubMed]
    [Google Scholar]
  27. Berčič RL, Cizelj I, Dušanić D, Narat M, Zorman-Rojs O et al. Neuraminidase of Mycoplasma synoviae desialylates heavy chain of the chicken immunoglobulin G and glycoproteins of chicken tracheal mucus. Avian Pathol 2011;40:299–308 [CrossRef][PubMed]
    [Google Scholar]
  28. May M, Brown DR. Genetic variation in sialidase and linkage to N-acetylneuraminate catabolism in Mycoplasma synoviae. Microb Pathog 2008;45:38–44 [CrossRef][PubMed]
    [Google Scholar]
  29. Sherblom AP, Bharathan S, Hall PJ, Smagula RM, Moody CE et al. Bovine serum sialic acid: age-related changes in type and content. Int J Biochem 1988;20:1177–1183 [CrossRef][PubMed]
    [Google Scholar]
  30. Marion C, Burnaugh AM, Woodiga SA, King SJ. Sialic acid transport contributes to pneumococcal colonization. Infect Immun 2011;79:1262–1269 [CrossRef][PubMed]
    [Google Scholar]
  31. Kim BS, Hwang J, Kim MH, Choi SH. Cooperative regulation of the Vibrio vulnificus nan gene cluster by NanR protein, cAMP receptor protein, and N-acetylmannosamine 6-phosphate. J Biol Chem 2011;286:40889–40899 [CrossRef][PubMed]
    [Google Scholar]
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