Diversity-Generating Machines: Genetics of Bacterial Sugar-Coating

Overview

Journal Trends Microbiol

Date 2018 Jul 25

PMID 30037568

Citations 59

Authors

Rafal J Mostowy

Kathryn E Holt

Affiliations

Soon will be listed here.

Abstract

Bacterial pathogens and commensals are surrounded by diverse surface polysaccharides which include capsules and lipopolysaccharides. These carbohydrates play a vital role in bacterial ecology and interactions with the environment. Here, we review recent rapid advancements in this field, which have improved our understanding of the roles, structures, and genetics of bacterial polysaccharide antigens. Genetic loci encoding the biosynthesis of these antigens may have evolved as bacterial diversity-generating machines, driven by selection from a variety of forces, including host immunity, bacteriophages, and cell-cell interactions. We argue that the high adaptive potential of polysaccharide antigens should be taken into account in the design of polysaccharide-targeting medical interventions like conjugate vaccines and phage-based therapies.

Citing Articles

Large diversity in the O-chain biosynthetic cluster within populations of Pelagibacterales.

Haro-Moreno J, Lopez-Perez M, Molina-Pardines C, Rodriguez-Valera F mBio. 2025; 16(3):e0345524.

PMID: 39969192 PMC: 11898729. DOI: 10.1128/mbio.03455-24.

Diagnosing and engineering gut microbiomes.

Cappio Barazzone E, Diard M, Hug I, Larsson L, Slack E EMBO Mol Med. 2024; 16(11):2660-2677.

PMID: 39468301 PMC: 11554810. DOI: 10.1038/s44321-024-00149-4.

Inter-individual and inter-regional variability of breast milk antibody reactivity to bacterial lipopolysaccharides.

Crone L, Sobek J, Muller N, Restin T, Bassler D, Paganini D Front Immunol. 2024; 15:1404192.

PMID: 39308863 PMC: 11412857. DOI: 10.3389/fimmu.2024.1404192.

Microbiota and B-1 B cell repertoire development in mice.

Stewart New J, Glenn King R, Foote J, Kearney J Curr Opin Immunol. 2024; 89:102452.

PMID: 39180941 PMC: 11365744. DOI: 10.1016/j.coi.2024.102452.

An exopolysaccharide pathway from a freshwater isolate.

Goetsch A, Ufearo D, Keiser G, Heiss C, Azadi P, Hershey D J Bacteriol. 2024; 206(8):e0016924.

PMID: 39007563 PMC: 11340318. DOI: 10.1128/jb.00169-24.

References

Levin B, Bull J . Population and evolutionary dynamics of phage therapy. Nat Rev Microbiol. 2004; 2(2):166-73. DOI: 10.1038/nrmicro822. View

Mostowy R, Croucher N, De Maio N, Chewapreecha C, Salter S, Turner P . Pneumococcal Capsule Synthesis Locus cps as Evolutionary Hotspot with Potential to Generate Novel Serotypes by Recombination. Mol Biol Evol. 2017; 34(10):2537-2554. PMC: 5850285. DOI: 10.1093/molbev/msx173. View

King S, Hippe K, Weiser J . Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol Microbiol. 2006; 59(3):961-74. DOI: 10.1111/j.1365-2958.2005.04984.x. View

Perrin A, Larsonneur E, Nicholson A, Edwards D, Gundlach K, Whitney A . Evolutionary dynamics and genomic features of the Elizabethkingia anophelis 2015 to 2016 Wisconsin outbreak strain. Nat Commun. 2017; 8:15483. PMC: 5458099. DOI: 10.1038/ncomms15483. View

Nielsen S, de Gier C, Dimopoulou C, Gupta V, Hansen L, Norskov-Lauritsen N . The capsule biosynthesis locus of Haemophilus influenzae shows conspicuous similarity to the corresponding locus in Haemophilus sputorum and may have been recruited from this species by horizontal gene transfer. Microbiology (Reading). 2015; 161(6):1182-8. DOI: 10.1099/mic.0.000081. View

Ingle D, Valcanis M, Kuzevski A, Tauschek M, Inouye M, Stinear T . serotyping of from short read data identifies limited novel O-loci but extensive diversity of O:H serotype combinations within and between pathogenic lineages. Microb Genom. 2017; 2(7):e000064. PMC: 5343136. DOI: 10.1099/mgen.0.000064. View

Zafar M, Hamaguchi S, Zangari T, Cammer M, Weiser J . Capsule Type and Amount Affect Shedding and Transmission of . mBio. 2017; 8(4). PMC: 5565965. DOI: 10.1128/mBio.00989-17. View

Schmid J, Sieber V, Rehm B . Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front Microbiol. 2015; 6:496. PMC: 4443731. DOI: 10.3389/fmicb.2015.00496. View

Kroll J, Moxon E . Capsulation in distantly related strains of Haemophilus influenzae type b: genetic drift and gene transfer at the capsulation locus. J Bacteriol. 1990; 172(3):1374-9. PMC: 208608. DOI: 10.1128/jb.172.3.1374-1379.1990. View

10.

Arnold J, Spacht D, Koudelka G . Determinants that govern the recognition and uptake of Escherichia coli O157 : H7 by Acanthamoeba castellanii. Cell Microbiol. 2016; 18(10):1459-70. DOI: 10.1111/cmi.12591. View

11.

Sukupolvi-Petty S, Grass S, St Geme 3rd J . The Haemophilus influenzae Type b hcsA and hcsB gene products facilitate transport of capsular polysaccharide across the outer membrane and are essential for virulence. J Bacteriol. 2006; 188(11):3870-7. PMC: 1482897. DOI: 10.1128/JB.01968-05. View

12.

Zarantonelli M, Huerre M, Taha M, Alonso J . Differential role of lipooligosaccharide of Neisseria meningitidis in virulence and inflammatory response during respiratory infection in mice. Infect Immun. 2006; 74(10):5506-12. PMC: 1594929. DOI: 10.1128/IAI.00655-06. View

13.

Minot S, Bryson A, Chehoud C, Wu G, Lewis J, Bushman F . Rapid evolution of the human gut virome. Proc Natl Acad Sci U S A. 2013; 110(30):12450-5. PMC: 3725073. DOI: 10.1073/pnas.1300833110. View

14.

Clark E, Emmadi M, Krupp K, Podilapu A, Helble J, Kulkarni S . Development of Rare Bacterial Monosaccharide Analogs for Metabolic Glycan Labeling in Pathogenic Bacteria. ACS Chem Biol. 2016; 11(12):3365-3373. PMC: 5161589. DOI: 10.1021/acschembio.6b00790. View

15.

Hammerschmidt S, Muller A, Sillmann H, Muhlenhoff M, Borrow R, Fox A . Capsule phase variation in Neisseria meningitidis serogroup B by slipped-strand mispairing in the polysialyltransferase gene (siaD): correlation with bacterial invasion and the outbreak of meningococcal disease. Mol Microbiol. 1996; 20(6):1211-20. DOI: 10.1111/j.1365-2958.1996.tb02641.x. View

16.

David S, Sanchez-Buso L, Harris S, Marttinen P, Rusniok C, Buchrieser C . Dynamics and impact of homologous recombination on the evolution of Legionella pneumophila. PLoS Genet. 2017; 13(6):e1006855. PMC: 5507463. DOI: 10.1371/journal.pgen.1006855. View

17.

Garbe J, Sjogren J, Cosgrave E, Struwe W, Bober M, Olin A . EndoE from Enterococcus faecalis hydrolyzes the glycans of the biofilm inhibiting protein lactoferrin and mediates growth. PLoS One. 2014; 9(3):e91035. PMC: 3946673. DOI: 10.1371/journal.pone.0091035. View

18.

Lipsitch M, OHagan J . Patterns of antigenic diversity and the mechanisms that maintain them. J R Soc Interface. 2007; 4(16):787-802. PMC: 2394542. DOI: 10.1098/rsif.2007.0229. View

19.

Bartley S, Mowlaboccus S, Mullally C, Stubbs K, Vrielink A, Maiden M . Acquisition of the capsule locus by horizontal gene transfer in Neisseria meningitidis is often accompanied by the loss of UDP-GalNAc synthesis. Sci Rep. 2017; 7:44442. PMC: 5349592. DOI: 10.1038/srep44442. View

20.

Kadioglu A, Weiser J, Paton J, Andrew P . The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol. 2008; 6(4):288-301. DOI: 10.1038/nrmicro1871. View