Effect of O-acetylation of O antigen of Escherichia coli lipopolysaccharide on the nonspecific barrier function of the outer membrane

Kulikov, Eugene E.; Majewska, Joanna; Prokhorov, Nikolai S.; Golomidova, Alla K.; Tatarskiy, E V; Letarov, Andrey V.

doi:10.1134/s0026261717030080

“…This includes gene functions for glycosyltransferases involved in lipopolysaccharide (LPS) biosynthesis (COG3306), peptidoglycan/LPS O -acetylase OafA/YrhL containing acyltransferase and SGNH-hydrolase domains (COG1835), and UDP-galactopyranose mutase (COG0562). LPS is a major component of Gram-negative bacterial cell walls that can be modified by glycosyltransferases and acyltransferases, and variations in the structure of LPS can provide selective advantages in different environments such as inhibiting bacteriophage binding, temperature tolerance, and antimicrobial resistance ( 92 – 95 ). Functional enrichment analyses in anvi’o identified the UDP-galactopyranose mutase COG function as present only in Nasonia -associated genomes ( q = 0.0173) and responsible for the biosynthesis of galactofuranose, a sugar structure found in bacterial cell walls that is absent in mammals ( 96 , 97 ) ( Table S6 ).…”

Section: Resultsmentioning

confidence: 99%

Genomes of Gut Bacteria from Nasonia Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown

Cross

¹

,

Leigh

²

,

Hatmaker

³

et al. 2021

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Phylosymbiosis is a cross-system trend whereby microbial community relationships recapitulate the host phylogeny. In Nasonia parasitoid wasps, phylosymbiosis occurs throughout development, is distinguishable between sexes, and benefits host development and survival. Moreover, the microbiome shifts in hybrids as a rare Proteus bacterium in the microbiome becomes dominant. The larval hybrids then catastrophically succumb to bacterium-assisted lethality and reproductive isolation between the species. Two important questions for understanding phylosymbiosis and bacterium-assisted lethality in hybrids are (i) do the Nasonia bacterial genomes differ from other animal isolates and (ii) are the hybrid bacterial genomes the same as those in the parental species? Here, we report the cultivation, whole-genome sequencing, and comparative analyses of the most abundant gut bacteria in Nasonia larvae, Providencia rettgeri and Proteus mirabilis. Characterization of new isolates shows Proteus mirabilis forms a more robust biofilm than Providencia rettgeri and that, when grown in coculture, Proteus mirabilis significantly outcompetes Providencia rettgeri. Providencia rettgeri genomes from Nasonia are similar to each other and more divergent from pathogenic, human associates. Proteus mirabilis from Nasonia vitripennis, Nasonia giraulti, and their hybrid offspring are nearly identical and relatively distinct from human isolates. These results indicate that members of the larval gut microbiome within Nasonia are most similar to each other, and the strain of the dominant Proteus mirabilis in hybrids is resident in parental species. Holobiont interactions between shared, resident members of the wasp microbiome and the host underpin phylosymbiosis and hybrid breakdown. IMPORTANCE Animal and plant hosts often establish intimate relationships with their microbiomes. In varied environments, closely related host species share more similar microbiomes, a pattern termed phylosymbiosis. When phylosymbiosis is functionally significant and beneficial, microbial transplants between host species and host hybridization can have detrimental consequences on host biology. In the Nasonia parasitoid wasp genus, which contains a phylosymbiotic gut community, both effects occur and provide evidence for selective pressures on the holobiont. Here, we show that bacterial genomes in Nasonia differ from other environments and harbor genes with unique functions that may regulate phylosymbiotic relationships. Furthermore, the bacteria in hybrids are identical to those in parental species, thus supporting a hologenomic tenet that the same members of the microbiome and the host genome impact phylosymbiosis, hybrid breakdown, and speciation.

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“…LPS molecules are comprised of lipid A, core oligosaccharide and O-antigen (or O-polysaccharide; OPS). These structures play a role in the interactions of bacteria with various surfaces and molecules, including other bacterial or eukaryotic cells 2 , immunity factors 3–5 , enzymes 6 , and bacteriophages 7 . Bacterial surface oligo- and polysaccharides also contribute to structural stability of the outer membrane that may be relevant to bacteriophage penetration 8–11 .…”

Section: Introductionmentioning

confidence: 99%

High-throughput LPS profiling as a tool for revealing of bacteriophage infection strategies

Kulikov

¹

,

Golomidova

²

,

Prokhorov

³

et al. 2019

Sci Rep

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O-antigens of Gram-negative bacteria modulate the interactions of bacterial cells with diverse external factors, including the components of the immune system and bacteriophages. Some phages need to acquire specific adhesins to overcome the O-antigen layer. For other phages, O-antigen is required for phage infection. In this case, interaction of phage receptor binding proteins coupled with enzymatic degradation or modification of the O-antigen is followed by phage infection. Identification of the strategies used by newly isolated phages may be of importance in their consideration for various applications. Here we describe an approach based on screening for host LPS alterations caused by selection by bacteriophages. We describe an optimized LPS profiling procedure that is simple, rapid and suitable for mass screening of mutants. We demonstrate that the phage infection strategies identified using a set of engineered E. coli 4 s mutants with impaired or altered LPS synthesis are in good agreement with the results of simpler tests based on LPS profiling of phage-resistant spontaneous mutants.

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“…This includes gene functions for glycosyltransferases involved in LPS biosynthesis (COG3306), peptidoglycan/LPS O-acetylase OafA/YrhL containing acyltransferase and SGNH-hydrolase domains (COG1835), and UDP-galactopyranose mutase (COG0562). LPS is a major component of Gram-negative bacterial cells walls that can be modified by glycosotransferases and acyltransferases, and variations in the structure of LPS can provide selective advantages in different environments such as inhibiting bacteriophage binding, temperature tolerance, and antimicrobial resistance [93–96]. Functional enrichment analyses in anvi’o identified the UDP-galactopyranose mutase COG function as only present in Nasonia -associated genomes (q=0.0173) and is responsible for the biosynthesis of galactofuranose, a sugar structure found in bacterial cell walls that is absent in mammals [97, 98] (Supplemental Table 6) .…”

Section: Resultsmentioning

confidence: 99%

Genomes of gut bacteria fromNasoniawasps shed light on phylosymbiosis and microbe-assisted hybrid breakdown

Cross

¹

,

Leigh

²

,

Hatmaker

³

et al. 2021

Preprint

0

View full text Add to dashboard Cite

Phylosymbiosis is a cross-system trend whereby microbial community relationships recapitulate the host phylogeny. In Nasonia parasitoid wasps, phylosymbiosis occurs throughout development, is distinguishable between sexes, and benefits host development and survival. Moreover, the microbiome shifts in hybrids as a rare Proteus bacteria in the microbiome becomes dominant. The larval hybrids then catastrophically succumb to bacterial-assisted lethality and reproductive isolation between the species. Two important questions for understanding phylosymbiosis and bacterial-assisted lethality in hybrids are: (i) Do the Nasonia bacterial genomes differ from other animal isolates and (ii) Are the hybrid bacterial genomes the same as those in the parental species? Here we report the cultivation, whole genome sequencing, and comparative analyses of the most abundant gut bacteria in Nasonia larvae, Providencia rettgeri and Proteus mirabilis. Characterization of new isolates shows Proteus mirabilis forms a more robust biofilm than Providencia rettgeri and when grown in co-culture, Proteus mirabilis significantly outcompetes Providencia rettgeri. Providencia rettgeri genomes from Nasonia are similar to each other and more divergent to pathogenic, human associates. Proteus mirabilis from N. vitripennis, N. giraulti, and their hybrid offspring are nearly identical and relatively distinct from human isolates based. These results indicate that members of the larval gut microbiome within Nasonia are most similar to each other, and the strain of the dominant Proteus mirabilis in hybrids is resident in parental species. Holobiont interactions between shared, resident members of the wasp microbiome and the host underpin phylosymbiosis and hybrid breakdown.

show abstract

Effect of O-acetylation of O antigen of Escherichia coli lipopolysaccharide on the nonspecific barrier function of the outer membrane

Cited by 11 publications

References 30 publications

Genomes of Gut Bacteria from Nasonia Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown

Genomes of Gut Bacteria from Nasonia Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown

High-throughput LPS profiling as a tool for revealing of bacteriophage infection strategies

Genomes of gut bacteria fromNasoniawasps shed light on phylosymbiosis and microbe-assisted hybrid breakdown

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