Diversity-Generating Machines: Genetics of Bacterial Sugar-Coating

Mostowy, Rafal; Holt, Kathryn E.

doi:10.1016/j.tim.2018.06.006

Cited by 97 publications

(100 citation statements)

References 121 publications

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“…In fact, the importance of surface structures (and especially the capsule on capsulated bacteria) on evolution, pathogenesis and host adaptation of bacterial pathogens is well known. However, full understanding on K-type variation has been hindered by variable drawbacks of available methods for K-typing, and reawakened only with the burst of genotypic or genomics-based approaches 17,36 . Nevertheless, the putative number of capsule types encountered varies strongly with the method used.…”

Section: Discussionmentioning

confidence: 99%

On the front line of Klebsiella pneumoniae surface structures understanding: establishment of Fourier Transform Infrared (FT-IR) spectroscopy as a capsule typing method

Rodrigues

Sousa

Lopes

et al. 2019

Preprint

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Genomics-based population analysis of multidrug resistant (MDR) Klebsiella pneumoniae (Kp) motivated a renewed interest on capsule (K) types given their importance as evolutionary and virulence markers of clinically relevant strains. However, there is a gap between genotypic based predictions and information on capsular polysaccharide structure and composition. We used molecular genotypic, comparative genomics, biochemical and phenotypic data on the cps locus to support the usefulness of Fourier-Transform Infrared (FT-IR) spectroscopy as a phenotypic approach for K-type characterization and identification. The approach was validated with a collection of representative MDR Kp isolates from main lineages/Clonal Groups (CGs) involved in local or nationwide epidemics in 6 European and South American countries. FT-IR-based K-type assignments were compared with those obtained by genotypic methods and WGS (cps operon), and further complemented with data on the polysaccharide composition and structure of known K-types.We demonstrate that our FT-IR-based spectroscopy approach can discriminate all 21 K-types identified with a resolution comparable (or even higher) to that provided by WGS, considered gold-standard methodology. Besides contributing to enlighten K-type diversity among a significant MDR Kp collection, the specific associations between certain K-types and Kp lineages identified in different geographic regions over time support the usefulness of our FT-IR-based approach for strain typing. Additionally, we demonstrate that FT-IR discriminatory ability is correlated with variation on the structure/composition of known K-types and, supported on WGS data, we were able to predict the sugar composition and chemical structure of new KL-types. Our data revealed an unprecedent resolution at a quick and low-cost rate of Kp K-types at the phenotypic level. Our FT-IR spectroscopy-based approach might be extremely useful not only as a cost-effective Kp typing tool, but also to improve our understanding on sugar-based coating structures of high relevance for strain evolution and host adaptation.

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Section: Discussionmentioning

confidence: 99%

On the front line of Klebsiella pneumoniae surface structures understanding: establishment of Fourier Transform Infrared (FT-IR) spectroscopy as a capsule typing method

Rodrigues

Sousa

Lopes

et al. 2019

Preprint

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“…We can expect the selective pressure from sIgA to foster strains with variation in surface antigen identity and indeed the majority of commensal bacteria are professionals at phase variation [48][49][50] (of note, this is likely driven by phage predation, 51,52 but can be repurposed for antibody evasion). Indeed one of the earliest observations of an effect of a monoclonal sIgA against B. thetaiotaomicron was to drive phase variation away from the targeted surface antigen.…”

Section: Critical Consequences Of Clumping: 1 Increased Clonal Extinmentioning

confidence: 99%

Growing, evolving and sticking in a flowing environment: understanding IgA interactions with bacteria in the gut

et al. 2019

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Summary Immunology research in the last 50 years has made huge progress in understanding the mechanisms of anti‐bacterial defense of deep, normally sterile, tissues such as blood, spleen and peripheral lymph nodes. In the intestine, with its dense commensal microbiota, it seems rare that this knowledge can be simply translated. Here we put forward the idea that perhaps it is not always the theory of immunology that is lacking to explain mucosal immunity, but rather that we have overlooked crucial parts of the mucosal immunological language required for its translation: namely intestinal and bacterial physiology. We will try to explain this in the context of intestinal secretory antibodies (mainly secretory IgA), which have been described to prevent, to alter, to not affect, or to promote colonization of the intestine and gut‐draining lymphoid tissues, and where effector mechanisms have remained elusive. In fact, these apparently contradictory outcomes can be generated by combining the basic premises of bacterial agglutination with an understanding of bacterial growth (i.e. secretory IgA‐driven enchained growth), fluid handling and bacterial competition in the gut lumen.

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“…Altogether, our study paints a picture of the evolutionary process shaping SP diversity in Enterobacteriales. It provides support for the idea that SP biosynthesis loci are diversity-generating machines, 304 optimised to produce novel phenotypes while minimising the fitness cost of producing sub-optimal combinations 33 . Diversity generated in such recombination hotspots is subject to action of various evolu-306 tionary forces that may di↵er from those shaping the structure of the underlying bacterial populations within which they occur.…”

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confidence: 99%

“…The inter-species view of SP genetics also highlights the range of possible factors that can shape the diversity and distribution of bacterial SPs. It is by now widely accepted that the SP loci are, at 268 least in some bacterial populations, under strong diversifying selection 33 . Indeed, diversifying selection is consistent with the enormous observed and predicted reservoirs of genetic diversity at SP loci (Fig.…”

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confidence: 99%

Diversity and evolution of surface polysaccharide synthesis loci in Enterobacteriales

Holt

Lassalle

Wick

et al. 2019

Preprint

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Bacterial capsules and lipopolysaccharides are diverse surface polysaccharides (SPs) that serve as the frontline for interactions with the outside world. While SPs can evolve rapidly, their diversity and evolutionary dynamics across different taxonomic scales has not been investigated in detail. Here, we focused on the bacterial order Enterobacteriales (including the medically-relevant Enterobacteriaceae), to carry out comparative genomics of two SP locus synthesis regions, cps and kps, using 27,334 genomes from 45 genera. We identified high-quality cps loci in 22 genera and kps in 11 genera, around 4% of which were detected in multiple species. We found SP loci to be highly dynamic genetic entities: their evolution was driven by high rates of horizontal gene transfer (HGT), both of whole loci and component genes, and relaxed purifying selection, yielding large repertoires of SP diversity. In spite of that, we found the presence of (near-)identical locus structures in distant taxonomic backgrounds that could not be explained by recent exchange, pointing to long-term selective preservation of locus structures in some populations. Our results reveal differences in evolutionary dynamics driving SP diversity within different bacterial species, with lineages of Escherichia coli, Enterobacter hormachei and Klebsiella aerogenes most likely to share SP loci via recent exchange; and lineages of Salmonella enterica, Citrobacter sakazakii and Serratia marcescens most likely to share SP loci via other mechanisms such as long-term preservation. Overall, the evolution of SP loci in Enterobacteriales is driven by a range of evolutionary forces and their dynamics and relative importance varies between different species.

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Diversity-Generating Machines: Genetics of Bacterial Sugar-Coating

Cited by 97 publications

References 121 publications

On the front line of Klebsiella pneumoniae surface structures understanding: establishment of Fourier Transform Infrared (FT-IR) spectroscopy as a capsule typing method

On the front line of Klebsiella pneumoniae surface structures understanding: establishment of Fourier Transform Infrared (FT-IR) spectroscopy as a capsule typing method

Growing, evolving and sticking in a flowing environment: understanding IgA interactions with bacteria in the gut

Diversity and evolution of surface polysaccharide synthesis loci in Enterobacteriales

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