O-antigens of bacteria of the genus Providencia: Structure, serology, genetics, and biosynthesis

Ovchinnikova, Olga G.; Różalski, Antoni; Liu, B.; Knirel, Yuriy A.

doi:10.1134/s0006297913070110

Cited by 23 publications

(22 citation statements)

References 87 publications

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“…S3 B , Supplementary Material online) resides within a cassette of four genes ( secB – gpsA – cysE – cspR ) right downstream of the O-antigen gene cluster, a frequently horizontally transferred structure (Wildschutte et al 2010; Ovchinnikova et al 2013). In lineage 4 Bartonella genomes, gpsA (Ar) seems to have been transferred singularly into a genomic region that is present in all bartonellae.…”

Section: Resultsmentioning

confidence: 99%

Horizontal Transfers and Gene Losses in the Phospholipid Pathway of Bartonella Reveal Clues about Early Ecological Niches

Zhu

Kosoy

Olival

et al. 2014

Genome Biology and Evolution

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Bartonellae are mammalian pathogens vectored by blood-feeding arthropods. Although of increasing medical importance, little is known about their ecological past, and host associations are underexplored. Previous studies suggest an influence of horizontal gene transfers in ecological niche colonization by acquisition of host pathogenicity genes. We here expand these analyses to metabolic pathways of 28 Bartonella genomes, and experimentally explore the distribution of bartonellae in 21 species of blood-feeding arthropods. Across genomes, repeated gene losses and horizontal gains in the phospholipid pathway were found. The evolutionary timing of these patterns suggests functional consequences likely leading to an early intracellular lifestyle for stem bartonellae. Comparative phylogenomic analyses discover three independent lineage-specific reacquisitions of a core metabolic gene—NAD(P)H-dependent glycerol-3-phosphate dehydrogenase (gpsA)—from Gammaproteobacteria and Epsilonproteobacteria. Transferred genes are significantly closely related to invertebrate Arsenophonus-, and Serratia-like endosymbionts, and mammalian Helicobacter-like pathogens, supporting a cellular association with arthropods and mammals at the base of extant Bartonella spp. Our studies suggest that the horizontal reacquisitions had a key impact on bartonellae lineage specific ecological and functional evolution.

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Section: Resultsmentioning

confidence: 99%

Horizontal Transfers and Gene Losses in the Phospholipid Pathway of Bartonella Reveal Clues about Early Ecological Niches

Zhu

Kosoy

Olival

et al. 2014

Genome Biology and Evolution

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“…Quip3N is an unusual deoxysugar, which has been observed in the O-antigens of various Gram-negative bacteria and in the S layers of glycoprotein glycans of some Gram-positive bacteria (64)(65)(66). Although rarely studied, Quip3N has also been found in the OSs of LOS class E, H, and P isolates in C. jejuni exclusively as an N-acetyl derivative (Quip3NAc) (54,(67)(68)(69).…”

Section: Discussionmentioning

confidence: 99%

Large Sequence Diversity within the Biosynthesis Locus and Common Biochemical Features of Campylobacter coli Lipooligosaccharides

et al. 2016

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Despite the importance of lipooligosaccharides (LOSs) in the pathogenicity of campylobacteriosis, little is known about the genetic and phenotypic diversity of LOS in Campylobacter coli. In this study, we investigated the distribution of LOS locus classes among a large collection of unrelated C. coli isolates sampled from several different host species. Furthermore, we paired C. coli genomic information and LOS chemical composition for the first time to investigate possible associations between LOS locus class sequence diversity and biochemical heterogeneity. After identifying three new LOS locus classes, only 85% of the 144 isolates tested were assigned to a class, suggesting higher genetic diversity than previously thought. This genetic diversity is at the basis of a completely unexplored LOS structural heterogeneity. Mass spectrometry analysis of the LOSs of nine isolates, representing four different LOS classes, identified two features distinguishing C. coli LOS from that of Campylobacter jejuni. 2-Amino-2-deoxy-D-glucose (GlcN)-GlcN disaccharides were present in the lipid A backbone, in contrast to the ␤-1=-6-linked 3-diamino-2,3-dideoxy-D-glucopyranose (GlcN3N)-GlcN backbone observed in C. jejuni. Moreover, despite the fact that many of the genes putatively involved in 3-acylamino-3,6-dideoxy-D-glucose (Quip3NAcyl) were apparently absent from the genomes of various isolates, this rare sugar was found in the outer core of all C. coli isolates. Therefore, regardless of the high genetic diversity of the LOS biosynthesis locus in C. coli, we identified species-specific phenotypic features of C. coli LOS that might explain differences between C. jejuni and C. coli in terms of population dynamics and host adaptation. IMPORTANCEDespite the importance of C. coli to human health and its controversial role as a causative agent of Guillain-Barré syndrome, little is known about the genetic and phenotypic diversity of C. coli LOSs. Therefore, we paired C. coli genomic information and LOS chemical composition for the first time to address this paucity of information. We identified two species-specific phenotypic features of C. coli LOS, which might contribute to elucidating the reasons behind the differences between C. jejuni and C. coli in terms of population dynamics and host adaptation. C ampylobacteriosis is the most common bacterial foodborne disease in developed countries, with over 200,000 human cases being reported annually in the European Union alone (1). The true burden of the disease in the population is likely underestimated, as many infections result in mild gastroenteritis (1). Approximately 80% of reported infections are caused by Campylobacter jejuni, and 7 to 18% of cases are attributed to C. coli. Therefore, C. coli is among the five most important bacterial etiological agents of human gastroenteritis (2, 3).As in other Gram-negative bacteria, Campylobacter species cell surface glycoconjugates, including lipooligosaccharides (LOSs), play an important role in serum and bile resistance; resistanc...

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“…Gram‐negative bacteria belonging to the genus Providencia can cause acute infections of the human urinary and gastrointestinal tracts, especially in immunocompromised individuals . These opportunistic pathogens, often found in polluted waters or sewage, have been isolated from a wide range of organisms including chickens, dogs, and cows.…”

Section: Introductionmentioning

confidence: 99%

Molecular structure of an N‐formyltransferase from Providencia alcalifaciensO30

et al. 2015

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The existence of N-formylated sugars in the O-antigens of Gram-negative bacteria has been known since the middle 1980s, but only recently have the biosynthetic pathways for their production been reported. In these pathways, glucose-1-phosphate is first activated by attachment to a dTMP moiety. This step is followed by a dehydration reaction and an amination. The last step in these pathways is catalyzed by N-formyltransferases that utilize N 10 -formyltetrahydrofolate as the carbon source. Here we describe the three-dimensional structure of one of these N-formyltransferases, namely VioF from Providencia alcalifaciens O30. Specifically, this enzyme catalyzes the conversion of dTDP-4-amino-4,6-dideoxyglucose (dTDP-Qui4N) to dTDP-4,6-dideoxy-4-formamido-Dglucose (dTDP-Qui4NFo). For this analysis, the structure of VioF was solved to 1.9 Å resolution in both its apoform and in complex with tetrahydrofolate and dTDP-Qui4N. The crystals used in the investigation belonged to the space group R32 and demonstrated reticular merohedral twinning. The overall catalytic core of the VioF subunit is characterized by a six stranded mixed b-sheet flanked on one side by three a-helices and on the other side by mostly random coil. This Nterminal domain is followed by an a-helix and a b-hairpin that form the subunit:subunit interface. The active site of the enzyme is shallow and solvent-exposed. Notably, the pyranosyl moiety of dTDP-Qui4N is positioned into the active site by only one hydrogen bond provided by Lys 77. Comparison of the VioF model to that of a previously determined N-formyltransferase suggests that substrate specificity is determined by interactions between the protein and the pyrophosphoryl group of the dTDP-sugar substrate.

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O-antigens of bacteria of the genus Providencia: Structure, serology, genetics, and biosynthesis

Cited by 23 publications

References 87 publications

Horizontal Transfers and Gene Losses in the Phospholipid Pathway of Bartonella Reveal Clues about Early Ecological Niches

Horizontal Transfers and Gene Losses in the Phospholipid Pathway of Bartonella Reveal Clues about Early Ecological Niches

Large Sequence Diversity within the Biosynthesis Locus and Common Biochemical Features of Campylobacter coli Lipooligosaccharides

Molecular structure of an N‐formyltransferase from Providencia alcalifaciensO30

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