1887

Abstract

Several monosaccharides constitute naturally occurring glycans, but it is uncertain whether they constitute a universal set like the alphabets of proteins and DNA. Based on the available experimental observations, it is hypothesized herein that the glycan alphabet is not universal. Data on the presence/absence of pathways for the biosynthesis of 55 monosaccharides in 12 939 completely sequenced archaeal and bacterial genomes are presented in support of this hypothesis. Pathways were identified by searching for homologues of biosynthesis pathway enzymes. Substantial variations were observed in the set of monosaccharides used by organisms belonging to the same phylum, genera and even species. Monosaccharides were grouped as common, less common and rare based on their prevalence in Archaea and Bacteria. It was observed that fewer enzymes are sufficient to biosynthesize monosaccharides in the common group. It appears that the common group originated before the formation of the three domains of life. In contrast, the rare group is confined to a few species in a few phyla, suggesting that these monosaccharides evolved much later. Fold conservation, as observed in aminotransferases and SDR (short-chain dehydrogenase reductase) superfamily members involved in monosaccharide biosynthesis, suggests neo- and sub-functionalization of genes led to the formation of the rare group monosaccharides. The non-universality of the glycan alphabet begets questions about the role of different monosaccharides in determining an organism’s fitness.

Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000452
2020-10-13
2021-07-31
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/11/mgen000452.html?itemId=/content/journal/mgen/10.1099/mgen.0.000452&mimeType=html&fmt=ahah

References

  1. Varki A. Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 1993; 3:97–130 [View Article][PubMed]
    [Google Scholar]
  2. Mostowy RJ, Croucher NJ, De Maio N, Chewapreecha C, Salter SJ et al. Pneumococcal capsule synthesis locus CPS as evolutionary hotspot with potential to generate novel serotypes by recombination. Mol Biol Evol 2017; 34:2537–2554 [View Article]
    [Google Scholar]
  3. Mostowy RJ, Holt KE. Diversity-generating machines: genetics of bacterial sugar-coating. Trends Microbiol 2018; 26:1008–1021 [View Article][PubMed]
    [Google Scholar]
  4. Gabius H-J, Roth J. An introduction to the sugar code. Histochem Cell Biol 2017; 147:111–117 [View Article][PubMed]
    [Google Scholar]
  5. Bravo D, Silva C, Carter JA, Hoare A, Álvarez SA et al. Growth-phase regulation of lipopolysaccharide O-antigen chain length influences serum resistance in serovars of Salmonella . J Med Microbiol 2008; 57:938–946 [View Article]
    [Google Scholar]
  6. Kalynych S, Morona R, Cygler M. Progress in understanding the assembly process of bacterial O-antigen. FEMS Microbiol Rev 2014; 38:1048–1065 [View Article][PubMed]
    [Google Scholar]
  7. Johannessen C, Koomey M, Børud B. Hypomorphic glycosyltransferase alleles and recoding at contingency loci influence glycan microheterogeneity in the protein glycosylation system of Neisseria species. J Bacteriol 2012; 194:5034–5043 [View Article][PubMed]
    [Google Scholar]
  8. Kaltner H, Abad-Rodríguez J, Corfield AP, Kopitz J, Gabius H-J. The sugar code: letters and vocabulary, writers, editors and readers and biosignificance of functional glycan-lectin pairing. Biochem J 2019; 476:2623–2655 [View Article][PubMed]
    [Google Scholar]
  9. Herget S, Toukach PV, Ranzinger R, Hull WE, Knirel YA et al. Statistical analysis of the Bacterial Carbohydrate Structure Data Base (BCSDB): characteristics and diversity of bacterial carbohydrates in comparison with mammalian glycans. BMC Struct Biol 2008; 8:35 [View Article][PubMed]
    [Google Scholar]
  10. Tello M, Jakimowicz P, Errey JC, Freel Meyers CL, Walsh CT et al. Characterisation of Streptomyces spheroides NovW and revision of its functional assignment to a dTDP-6-deoxy-D-xylo-4-hexulose 3-epimerase. Chem Commun 2006; 10:1079–1081 [View Article][PubMed]
    [Google Scholar]
  11. Polizzi SJ, Walsh RM, Peeples WB, Lim J-M, Wells L et al. Human UDP-α-D-xylose synthase and Escherichia coli ArnA conserve a conformational shunt that controls whether xylose or 4-keto-xylose is produced. Biochemistry 2012; 51:8844–8855 [View Article][PubMed]
    [Google Scholar]
  12. Li Z, Mukherjee T, Bowler K, Namdari S, Snow Z et al. A four-gene operon in Bacillus cereus produces two rare spore-decorating sugars. J Biol Chem 2017; 292:7636–7650 [View Article][PubMed]
    [Google Scholar]
  13. Hwang S, Aronov A, Bar-Peled M. The biosynthesis of UDP-d-QuiNAc in Bacillus cereus ATCC 14579. PLoS One 2015; 10:e0133790 [View Article][PubMed]
    [Google Scholar]
  14. Ohno S. Evolution by Gene Duplication New York: Springer; 2013
    [Google Scholar]
  15. Copley SD. Evolution of new enzymes by gene duplication and divergence. FEBS J 2020; 287:1262–1283 [View Article][PubMed]
    [Google Scholar]
  16. Keinhörster D, George SE, Weidenmaier C, Wolz C. Function and regulation of Staphylococcus aureus wall teichoic acids and capsular polysaccharides. Int J Med Microbiol 2019; 309:151333 [View Article][PubMed]
    [Google Scholar]
  17. Pfannkuch L, Hurwitz R, Traulsen J, Sigulla J, Poeschke M et al. ADP heptose, a novel pathogen-associated molecular pattern identified in Helicobacter pylori . FASEB J 2019; 33:9087–9099 [View Article][PubMed]
    [Google Scholar]
  18. Trachtenberg S. Mollicutes-wall-less bacteria with internal cytoskeletons. J Struct Biol 1998; 124:244–256 [View Article][PubMed]
    [Google Scholar]
  19. Khachane AN, Timmis KN, Martins dos Santos VAP. Dynamics of reductive genome evolution in mitochondria and obligate intracellular microbes. Mol Biol Evol 2007; 24:449–456 [View Article][PubMed]
    [Google Scholar]
  20. Amano K, Tamura A, Ohashi N, Urakami H, Kaya S et al. Deficiency of peptidoglycan and lipopolysaccharide components in Rickettsia tsutsugamushi . Infect Immun 1987; 55:2290–2292 [View Article][PubMed]
    [Google Scholar]
  21. Rund S, Lindner B, Brade H, Holst O. Structural analysis of the lipopolysaccharide from Chlamydia trachomatis serotype L2. J Biol Chem 1999; 274:16819–16824 [View Article][PubMed]
    [Google Scholar]
  22. Peturova M, Vitiazeva V, Toman R. Structural features of the O-antigen of Rickettsia typhi, the etiological agent of endemic typhus. Acta Virol 2015; 59:228–233 [View Article][PubMed]
    [Google Scholar]
  23. Theunissen C, Cnops L, Van Esbroeck M, Huits R, Bottieau E. Acute-phase diagnosis of murine and scrub typhus in Belgian travelers by polymerase chain reaction: a case report. BMC Infect Dis 2017; 17:273 [View Article][PubMed]
    [Google Scholar]
  24. Tamura A, Ohashi N, Urakami H, Miyamura S. Classification of Rickettsia tsutsugamushi in a new genus, Orientia gen. nov., as Orientia tsutsugamushi comb. nov. Int J Syst Bacteriol 1995; 45:589–591 [View Article][PubMed]
    [Google Scholar]
  25. Fuxelius H-H, Darby A, Min C-K, Cho N-H, Andersson SGE. The genomic and metabolic diversity of Rickettsia . Res Microbiol 2007; 158:745–753 [View Article][PubMed]
    [Google Scholar]
  26. Moissl-Eichinger C, Pausan M, Taffner J, Berg G, Bang C et al. Archaea are interactive components of complex microbiomes. Trends Microbiol 2018; 26:70–85 [View Article][PubMed]
    [Google Scholar]
  27. Lurie-Weinberger MN, Peeri M, Gophna U. Contribution of lateral gene transfer to the gene repertoire of a gut-adapted methanogen. Genomics 2012; 99:52–58 [View Article][PubMed]
    [Google Scholar]
  28. Lukácová M, Barák I, Kazár J. Role of structural variations of polysaccharide antigens in the pathogenicity of Gram-negative bacteria. Clin Microbiol Infect 2008; 14:200–206 [View Article][PubMed]
    [Google Scholar]
  29. Hassler CS, Schoemann V, Nichols CM, Butler ECV, Boyd PW. Saccharides enhance iron bioavailability to Southern Ocean phytoplankton. Proc Natl Acad Sci USA 2011; 108:1076–1081 [View Article][PubMed]
    [Google Scholar]
  30. Zhang Z, Chen Y, Wang R, Cai R, Fu Y et al. The fate of marine bacterial exopolysaccharide in natural marine microbial communities. PLoS ONE 2015; 10:e0142690
    [Google Scholar]
  31. Qimron U, Marintcheva B, Tabor S, Richardson CC. Genomewide screens for Escherichia coli genes affecting growth of T7 bacteriophage. Proc Natl Acad Sci USA 2006; 103:19039–19044 [View Article][PubMed]
    [Google Scholar]
  32. Morrison MJ, Imperiali B. The renaissance of bacillosamine and its derivatives: pathway characterization and implications in pathogenicity. Biochemistry 2014; 53:624–638 [View Article][PubMed]
    [Google Scholar]
  33. Wacker M, Feldman MF, Callewaert N, Kowarik M, Clarke BR et al. Substrate specificity of bacterial oligosaccharyltransferase suggests a common transfer mechanism for the bacterial and eukaryotic systems. Proc Natl Acad Sci USA 2006; 103:7088–7093 [View Article]
    [Google Scholar]
  34. Kenyon JJ, Cunneen MM, Reeves PR. Genetics and evolution of Yersinia pseudotuberculosis O-specific polysaccharides: a novel pattern of O-antigen diversity. FEMS Microbiol Rev 2017; 41:200–217 [View Article][PubMed]
    [Google Scholar]
  35. Skurnik M, Peippo A, Ervelä E. Characterization of the O-antigen gene clusters of Yersinia pseudotuberculosis and the cryptic O-antigen gene cluster of Yersinia pestis shows that the plague Bacillus is most closely related to and has evolved from Y. pseudotuberculosis serotype O:1b. Mol Microbiol 2000; 37:316–330 [View Article][PubMed]
    [Google Scholar]
  36. Xu Y, Brenning B, Clifford A, Vollmer D, Bearss J et al. Discovery of novel putative inhibitors of UDP-GlcNAc 2-epimerase as potent antibacterial agents. ACS Med Chem Lett 2013; 4:1142–1147 [View Article][PubMed]
    [Google Scholar]
  37. Mariño K, Bones J, Kattla JJ, Rudd PM. A systematic approach to protein glycosylation analysis: a path through the maze. Nat Chem Biol 2010; 6:713–723 [View Article][PubMed]
    [Google Scholar]
  38. Varki A. Biological roles of glycans. Glycobiology 2017; 27:3–49 [View Article][PubMed]
    [Google Scholar]
  39. Malmström A, Bartolini B, Thelin MA, Pacheco B, Maccarana M. Iduronic acid in chondroitin/dermatan sulfate: biosynthesis and biological function. J Histochem Cytochem 2012; 60:916–925 [View Article][PubMed]
    [Google Scholar]
  40. Jones C. Revised structures for the capsular polysaccharides from Staphylococcus aureus types 5 and 8, components of novel glycoconjugate vaccines. Carbohydr Res 2005; 340:1097–1106 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000452
Loading
/content/journal/mgen/10.1099/mgen.0.000452
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error