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Bacterial Carbohydrates: Structures, Applications, and Structure/Activity Relationships

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Microbiology".

Deadline for manuscript submissions: closed (31 January 2021) | Viewed by 33379

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Prof. Dr. Maria Michela Corsaro

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Department of Chemical Science, University of Naples Federico II, Naples, Italy
Interests: polysaccharides and oligosaccharides; glycolipids; extremophiles; secondary metabolites; structural elucidation; NMR spectroscopy; mass spectrometry; anti-biofilm molecules
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Dear colleagues,

Bacteria is a domain of Prokaryotic microorganisms. Some of them are pathogens, responsible of several human serious diseases, like cholera, tuberculosis, and anthrax. Others are commensal or even beneficial for humans, such as those inhabiting our gut. In addition, microbial diversity in some extreme ecosystems revealed to be an untapped reservoir of bioactive small molecules and polymers, also due to the increasing biotechnological request for new safely products. Among these, the bacterial polysaccharides are of overwhelming importance. The bacterial polysaccharides include cell-wall polymers, such as lipopolysaccharides (LPSs), extracellular polymers, both exopolysaccharides (EPSs) and capsular (CPSs), and intracellular polymers. The different matrices where they are embedded, like cells, growth media, biofilms and extracellular vesicles, necessitate different challenges during the purification steps. Finally, the high grade of variability about the polysaccharides primary structure makes this work tricky and fascinating. Bacterial carbohydrates polymers are involved in many cellular functions and host-interaction relationships. However, their structural determination is still a challenge for chemists. In addition, the knowledge of the structure is fundamental for their possible application.

The aim of this Special Issue is to collect, as many as possible papers addressing the structural determination of bacterial carbohydrates polymers, the methodologies for their purification and structural characterization, and their application in food and pharmaceutical fields. Both reviews and original research papers are appreciated. In addition, reviews and discussion papers underlying problems and drawing future perspectives about the methodologies used for establishing carbohydrates structures/activity relationships are especially invited.

Prof. Dr. Maria Michela Corsaro
Guest Editor

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Keywords

Structural determination
Carbohydrates polymers
NMR spectroscopy
Mass Spectrometry
Biological activity
Structure/activity relationship
Polysaccharides
Biofilm
Extracellular membrane vesicles polysaccharides

Published Papers (11 papers)

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Research

10 pages, 1916 KiB

Open AccessArticle

Complete Characterization of the O-Antigen from the LPS of Aeromonas bivalvium

by Rossella Di Guida, Angela Casillo, Juan M. Tomás, Susana Merino and Maria Michela Corsaro

Int. J. Mol. Sci. 2022, 23(3), 1204; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23031204 - 21 Jan 2022

Cited by 3 | Viewed by 1881

Abstract

Aeromonas species are found in the aquatic environment, drinking water, bottled mineral water, and different types of foods, such as meat, fish, seafood, or vegetables. Some of these species are primary or opportunistic pathogens for invertebrates and vertebrates, including humans. Among the pathogenic factors associated with these species, there are the lipopolysaccharides (LPSs). LPSs are the major components of the external leaflet of Gram-negative bacterial outer membrane. LPS is a glycoconjugate, generally composed of three portions: lipid A, core oligosaccharide, and O-specific polysaccharide or O-antigen. The latter, which may be present (smooth LPS) or not (rough LPS), is the most exposed part of the LPS and is involved in the pathogenicity by protecting infecting bacteria from serum complement killing and phagocytosis. The O-antigen is a polymer of repeating oligosaccharide units with high structural variability, particularly the terminal sugar, that confers the immunological specificity to the O-antigen. In this study, we established the structure of the O-chain repeating unit of the LPS from Aeromonas bivalvium strain 868 E^T (=CECT 7113^T = LMG 23376^T), a mesophilic bacterium isolated from cockles (Cardium sp.) and obtained from a retail market in Barcelona (Spain), whose biosynthesis core LPS cluster does not contain the waaE gene as most of Aeromonas species. After mild acid hydrolysis, the lipid A was removed by centrifugation and the obtained polysaccharide was fully characterized by chemical analysis and NMR spectroscopy. The polymer consists of a heptasaccharide repeating unit containing D-GalNAc, L-Rha, D-GlcNAc, and D-FucNAc residues. Full article

(This article belongs to the Special Issue Bacterial Carbohydrates: Structures, Applications, and Structure/Activity Relationships)

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16 pages, 2879 KiB

Open AccessArticle

Carbon Source-Dependent Changes of the Structure of Streptococcus pneumoniae Capsular Polysaccharide with Serotype 6F

by Joel P. Werren, Lukas J. Troxler, Oluwaseun Rume-Abiola Oyewole, Alban Ramette, Silvio D. Brugger, Rémy Bruggmann, Mark van der Linden, Moon H. Nahm, Ilche Gjuroski, Carlo Casanova, Julien Furrer and Markus Hilty

Int. J. Mol. Sci. 2021, 22(9), 4580; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22094580 - 27 Apr 2021

Cited by 2 | Viewed by 3859

Abstract

The structure of the exopolysaccharide capsule of Streptococcus pneumoniae is defined by the genetic arrangement of the capsule operon allowing the unequivocal identification of the pneumococcal serotype. Here, we investigated the environment-dependent composition of the polysaccharide structure of S. pneumoniae serotype 6F. When grown in a chemically defined medium (CDM) with glucose versus galactose, the exopolysaccharide capsule of the serotype 6F strains reveals a ratio of 1/0.6 or 1/0.3 for galactose/glucose in the capsule by ¹H-NMR analyses, respectively. Increased production of the capsule precursor UDP-glucose has been identified by ³¹P-NMR in CDM with glucose. Flow cytometric experiments using monoclonal antibodies showed decreased labelling of Hyp6AG4 (specific for serotype 6A) antibodies when 6F is grown in glucose as compared to galactose, which mirrors the 1H-NMR results. Whole-genome sequencing analyses of serotype 6F isolates suggested that the isolates evolved during two different events from serotype 6A during the time when the 13-valent pneumococcal conjugate vaccine (PCV-13) was introduced. In conclusion, this study shows differences in the capsular structure of serotype 6F strains using glucose as compared to galactose as the carbon source. Therefore, 6F strains may show slightly different polysaccharide composition while colonizing the human nasopharynx (galactose rich) as compared to invasive locations such as the blood (glucose rich). Full article

(This article belongs to the Special Issue Bacterial Carbohydrates: Structures, Applications, and Structure/Activity Relationships)

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20 pages, 5326 KiB

Open AccessArticle

Structural Studies of the Lipopolysaccharide of Aeromonas veronii bv. sobria Strain K133 Which Represents New Provisional Serogroup PGO1 Prevailing among Mesophilic Aeromonads on Polish Fish Farms

by Katarzyna Dworaczek, Maria Kurzylewska, Magdalena Laban, Dominika Drzewiecka, Agnieszka Pękala-Safińska and Anna Turska-Szewczuk

Int. J. Mol. Sci. 2021, 22(8), 4272; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22084272 - 20 Apr 2021

Cited by 6 | Viewed by 2046

Abstract

In the present work, we performed immunochemical studies of LPS, especially the O-specific polysaccharide (O-PS) of Aeromonas veronii bv. sobria strain K133, which was isolated from the kidney of carp (Cyprinus carpio L.) during an outbreak of motile aeromonad infection/motile aeromonad septicemia (MAI/MAS) on a Polish fish farm. The structural characterization of the O-PS, which was obtained by mild acid degradation of the LPS, was performed with chemical methods, MALDI-TOF mass spectrometry, and ¹H and ¹³C NMR spectroscopy. It was revealed that the O-PS has a unique composition of a linear tetrasaccharide repeating unit and contains a rarely occurring sugar 2,4-diamino-2,4,6-trideoxy-D-glucose (bacillosamine), which may determine the specificity of the serogroup. Western blotting and ELISA confirmed that A. veronii bv. sobria strain K133 belongs to the new serogroup PGO1, which is one of the most commonly represented immunotypes among carp and trout isolates of Aeromonas sp. in Polish aquacultures. Considering the increase in the MAI/MAS incidences and their impact on freshwater species, also with economic importance, and in the absence of an effective immunoprophylaxis, studies of the Aeromonas O-antigens are relevant in the light of epidemiological data and monitoring emergent pathogens representing unknown antigenic variants and serotypes. Full article

(This article belongs to the Special Issue Bacterial Carbohydrates: Structures, Applications, and Structure/Activity Relationships)

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18 pages, 3731 KiB

Open AccessArticle

Analysis of the Structure and Biosynthesis of the Lipopolysaccharide Core Oligosaccharide of Pseudomonas syringae pv. tomato DC3000

by Alexander Kutschera, Ursula Schombel, Dominik Schwudke, Stefanie Ranf and Nicolas Gisch

Int. J. Mol. Sci. 2021, 22(6), 3250; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22063250 - 23 Mar 2021

Cited by 5 | Viewed by 2655

Abstract

Lipopolysaccharide (LPS), the major component of the outer membrane of Gram-negative bacteria, is important for bacterial viability in general and host–pathogen interactions in particular. Negative charges at its core oligosaccharide (core-OS) contribute to membrane integrity through bridging interactions with divalent cations. The molecular structure and synthesis of the core-OS have been resolved in various bacteria including the mammalian pathogen Pseudomonas aeruginosa. A few core-OS structures of plant-associated Pseudomonas strains have been solved to date, but the genetic components of the underlying biosynthesis remained unclear. We conducted a comparative genome analysis of the core-OS gene cluster in Pseudomonas syringae pv. tomato (Pst) DC3000, a widely used model pathogen in plant–microbe interactions, within the P. syringae species complex and to other plant-associated Pseudomonas strains. Our results suggest a genetic and structural conservation of the inner core-OS but variation in outer core-OS composition within the P. syringae species complex. Structural analysis of the core-OS of Pst DC3000 shows an uncommonly high phosphorylation and presence of an O-acetylated sugar. Finally, we combined the results of our genomic survey with available structure information to estimate the core-OS composition of other Pseudomonas species. Full article

(This article belongs to the Special Issue Bacterial Carbohydrates: Structures, Applications, and Structure/Activity Relationships)

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22 pages, 1588 KiB

Open AccessArticle

Exopolysaccharide Carbohydrate Structure and Biofilm Formation by Rhizobium leguminosarum bv. trifolii Strains Inhabiting Nodules of Trifoliumrepens Growing on an Old Zn–Pb–Cd-Polluted Waste Heap Area

by Ewa Oleńska, Wanda Małek, Urszula Kotowska, Jerzy Wydrych, Weronika Polińska, Izabela Swiecicka, Sofie Thijs and Jaco Vangronsveld

Int. J. Mol. Sci. 2021, 22(6), 2808; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22062808 - 10 Mar 2021

Cited by 11 | Viewed by 2694

Abstract

Heavy metals polluting the 100-year-old waste heap in Bolesław (Poland) are acting as a natural selection factor and may contribute to adaptations of organisms living in this area, including Trifolium repens and its root nodule microsymbionts—rhizobia. Exopolysaccharides (EPS), exuded extracellularly and associated with bacterial cell walls, possess variable structures depending on environmental conditions; they can bind metals and are involved in biofilm formation. In order to examine the effects of long-term exposure to metal pollution on EPS structure and biofilm formation of rhizobia, Rhizobium leguminosarum bv. trifolii strains originating from the waste heap area and a non-polluted reference site were investigated for the characteristics of the sugar fraction of their EPS using gas chromatography mass-spectrometry and also for biofilm formation and structural characteristics using confocal laser scanning microscopy under control conditions as well as when exposed to toxic concentrations of zinc, lead, and cadmium. Significant differences in EPS structure, biofilm thickness, and ratio of living/dead bacteria in the biofilm were found between strains originating from the waste heap and from the reference site, both without exposure to metals and under metal exposure. Received results indicate that studied rhizobia can be assumed as potentially useful in remediation processes. Full article

(This article belongs to the Special Issue Bacterial Carbohydrates: Structures, Applications, and Structure/Activity Relationships)

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15 pages, 1907 KiB

Open AccessArticle

Conserved Structural Features of Core Oligosaccharides among the Lipopolysaccharides of Respiratory Pathogens from the Genus Bordetella Analyzed Exclusively by NMR Spectroscopy

by Karolina Ucieklak, Sabina Koj and Tomasz Niedziela

Int. J. Mol. Sci. 2021, 22(3), 1029; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22031029 - 21 Jan 2021

Cited by 4 | Viewed by 1925

Abstract

Bacterial pathogens expose on the cell surface a variety of complex carbohydrate molecules. Gram-negative bacteria produce lipopolysaccharides, which are the main components of the outer membrane of bacterial envelopes and play a major role in host–pathogen interactions. B. pertussis, B. parapertussis, B. bronchiseptica, and B. holmesii, are mammalian respiratory pathogens, having substantial economic impact on human health and agriculture. B. pertussis is responsible for whooping cough (pertussis) and B. holmesii is the second pertussis etiological factor, but the current anti-pertussis vaccines do not provide cross-protection. The structural data on any given hypothetical carbohydrate antigen is a prerequisite for further analysis of structure-related activities and their interaction with hosts. ¹H NMR spectra constitute fingerprints of the analyzed glycans and provide unique identity information. The concept of structure-reporter groups has now been augmented by ¹H,¹³C-correlation spectra of the Bordetella oligosaccharides. The comparative analysis of Bordetellae oligosaccharides (OS) revealed that the hexasaccharide, comprising the α-GlcpN, α-GlcpA, 4,6-disubstituted-β-Glcp, 2,7-disubstituted-l-α-d-Hepp, 3,4-disubstituted-l-α-d-Hepp, and Kdo, constitute the least variable OS segment. This minimal common element in the structure of lipopolysaccharides of Bordetellae could be used to devise a universal cross-protective vaccine component against infections with various bacteria from the genus Bordetella. Full article

(This article belongs to the Special Issue Bacterial Carbohydrates: Structures, Applications, and Structure/Activity Relationships)

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16 pages, 3833 KiB

Open AccessArticle

A New Look at the Enterobacterial Common Antigen Forms Obtained during Rough Lipopolysaccharides Purification

by Tomasz K Gozdziewicz, Anna Maciejewska, Alona Tsybulska, Czeslaw Lugowski and Jolanta Lukasiewicz

Int. J. Mol. Sci. 2021, 22(2), 701; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22020701 - 12 Jan 2021

Cited by 2 | Viewed by 2433

Abstract

Enterobacterial common antigen (ECA) is a conserved antigen expressed by enterobacteria. It is built by trisaccharide repeating units: →3)-α-D-Fucp4NAc-(1→4)-β-D-ManpNAcA-(1→4)-α-D-GlcpNAc-(1→ and occurs in three forms: as surface-bound linear polysaccharides linked to a phosphoglyceride (ECA_PG) or lipopolysaccharide − endotoxin (ECA_LPS), and cyclic form (ECA_CYC). ECA maintains, outer membrane integrity, immunogenicity, and viability of enterobacteria. A supernatant obtained after LPS ultracentrifugation was reported as a source for ECA isolation, but it has never been assessed for detailed composition besides ECA_CYC. We used mild acid hydrolysis and gel filtration, or zwitterionic-hydrophilic interaction liquid (ZIC^®HILIC) chromatography combined with mass spectrometry for purification, fractionation, and structural analysis of rough Shigella sonnei and Escherichia coli R1 and K12 crude LPS preparations. Presented work is the first report concerning complex characteristic of all ECA forms present in LPS-derived supernatants. We demonstrated high heterogeneity of the supernatant-derived ECA that contaminate LPS purified by ultracentrifugation. Not only previously reported O-acetylated tetrameric, pentameric, and hexameric ECA_CYC have been identified, but also devoid of lipid moiety linear ECA built from 7 to 11 repeating units. Described results were common for all selected strains. The origin of linear ECA is discussed against the current knowledge about ECA_PG and ECA_LPS. Full article

(This article belongs to the Special Issue Bacterial Carbohydrates: Structures, Applications, and Structure/Activity Relationships)

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16 pages, 3414 KiB

Open AccessArticle

Glyceraldehyde-3-Phosphate Dehydrogenase Increases the Adhesion of Lactobacillus reuteri to Host Mucin to Enhance Probiotic Effects

by Zhaoxi Deng, Tian Dai, Wenming Zhang, Junli Zhu, Xin M. Luo, Dongyan Fu, Jianxin Liu and Haifeng Wang

Int. J. Mol. Sci. 2020, 21(24), 9756; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21249756 - 21 Dec 2020

Cited by 17 | Viewed by 2944

Abstract

The ability to adhere to the intestinal mucus layer is an important property of probiotic bacteria. Lactobacillus reuteri strains ZJ615 and ZJ617 show low and high adhesion, respectively, to intestinal epithelial cells. In this study, we quantified bacterial cell wall-associated glyceraldehyde-3-phosphate dehydrogenases (cw-GAPDH) and bacterial cell membrane permeability in both strains using immunoblotting and flow cytometry, respectively. Highly adhesive L. reuteri ZJ617 possessed significantly more cw-GAPDH, higher cell membrane permeability, and significantly higher adhesive ability toward mucin compared with low-adhesive L. reuteri ZJ615. In vitro adhesion studies and analysis of interaction kinetics using the Octet, the system revealed significantly decreased interaction between L. reuteri and mucin when mucin was oxidized when bacterial surface proteins were removed when bacteria were heat-inactivated at 80 °C for 30 min, and when the interaction was blocked with an anti-GAPDH antibody. SWISS-MODEL analysis suggested intensive interactions between mucin glycans (GalNAcα1-O-Ser, GalNAcαSer, and Galβ3GalNAc) and GAPDH. Furthermore, in vivo studies revealed significantly higher numbers of bacteria adhering to the jejunum, ileum, and colon of piglets orally inoculated with L. reuteri ZJ617 compared with those inoculated with L. reuteri ZJ615; this led to a significantly decreased rate of diarrhea in piglets inoculated with L. reuteri ZJ617. In conclusion, there are strong correlations among the abundance of cw-GAPDH in L. reuteri, the ability of the bacterium to adhere to the host, and the health benefits of this probiotic. Full article

(This article belongs to the Special Issue Bacterial Carbohydrates: Structures, Applications, and Structure/Activity Relationships)

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17 pages, 3202 KiB

Open AccessArticle

Bordetella holmesii Lipopolysaccharide Hide and Seek Game with Pertussis: Structural Analysis of the O-Specific Polysaccharide and the Core Oligosaccharide of the Type Strain ATCC 51541

by Karolina Ucieklak, Sabina Koj and Tomasz Niedziela

Int. J. Mol. Sci. 2020, 21(17), 6433; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21176433 - 03 Sep 2020

Cited by 6 | Viewed by 2818

Abstract

Whooping cough is a highly contagious disease caused predominantly by Bordetella pertussis, but it also comprises of a pertussis-like illness caused by B. holmesii. The virulence factors of B. holmesii and their role in the pathogenesis remain unknown. Lipopolysaccharide is the main surface antigen of all Bordetellae. Data on the structural features of the lipopolysaccharide (LPS) of B. holmesii are scarce. The poly- and oligosaccharide components released by mild acidic hydrolysis of the LPS were separated and investigated by ¹H and ¹³C NMR spectroscopy, mass spectrometry, and chemical methods. The structures of the O-specific polysaccharide and the core oligosaccharide of B. holmesii ATCC 51541 have been identified for the first time. The novel pentasaccharide repeating unit of the B. holmesii O-specific polysaccharide has the following structure: {→2)-α-l-Rhap-(1→6)-α-d-Glcp-(1→4)-[β-d-GlcpNAc-(1→3]-α-d-Galp-(1→3)-α-d-GlcpNAc-(1→}_n. The SDS-PAGE and serological cross-reactivities of the B. holmesii LPS suggested the similarity between the core oligosaccharides of B. holmesii ATCC 51541 and B. pertussis strain 606. The main oligosaccharide fraction contained a nonasaccharide. The comparative analysis of the NMR spectra of B. holmesii core oligosaccharide fraction with this of the B. pertussis strain 606 indicated that the investigated core oligosaccharides were identical. Full article

(This article belongs to the Special Issue Bacterial Carbohydrates: Structures, Applications, and Structure/Activity Relationships)

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22 pages, 7717 KiB

Open AccessArticle

Lipopolysaccharide-Linked Enterobacterial Common Antigen (ECA_LPS) Occurs in Rough Strains of Escherichia coli R1, R2, and R4

by Anna Maciejewska, Marta Kaszowska, Wojciech Jachymek, Czeslaw Lugowski and Jolanta Lukasiewicz

Int. J. Mol. Sci. 2020, 21(17), 6038; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21176038 - 21 Aug 2020

Cited by 23 | Viewed by 3079

Abstract

Enterobacterial common antigen (ECA) is a conserved surface antigen characteristic for Enterobacteriaceae. It is consisting of trisaccharide repeating unit, →3)-α-d-Fucp4NAc-(1→4)-β-d-ManpNAcA-(1→4)-α-d-GlcpNAc-(1→, where prevailing forms include ECA linked to phosphatidylglycerol (ECA_PG) and cyclic ECA (ECA_CYC). Lipopolysaccharide (LPS)-associated form (ECA_LPS) has been proved to date only for rough Shigella sonnei phase II. Depending on the structure organization, ECA constitutes surface antigen (ECA_PG and ECA_LPS) or maintains the outer membrane permeability barrier (ECA_CYC). The existence of LPS was hypothesized in the 1960–80s on the basis of serological observations. Only a few Escherichia coli strains (i.e., R1, R2, R3, R4, and K-12) have led to the generation of anti-ECA antibodies upon immunization, excluding ECA_PG as an immunogen and conjecturing ECA_LPS as the only immunogenic form. Here, we presented a structural survey of ECA_LPS in E. coli R1, R2, R3, and R4 to correlate previous serological observations with the presence of ECA_LPS. The low yields of ECA_LPS were identified in the R1, R2, and R4 strains, where ECA occupied outer core residues of LPS that used to be substituted by O-specific polysaccharide in the case of smooth LPS. Previously published observations and hypotheses regarding the immunogenicity and biosynthesis of ECA_LPS were discussed and correlated with presented herein structural data. Full article

(This article belongs to the Special Issue Bacterial Carbohydrates: Structures, Applications, and Structure/Activity Relationships)

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20 pages, 7520 KiB

Open AccessArticle

The FT-IR and Raman Spectroscopies as Tools for Biofilm Characterization Created by Cariogenic Streptococci

by Barbara Gieroba, Mikolaj Krysa, Kinga Wojtowicz, Adrian Wiater, Małgorzata Pleszczyńska, Michał Tomczyk and Anna Sroka-Bartnicka

Int. J. Mol. Sci. 2020, 21(11), 3811; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21113811 - 27 May 2020

Cited by 66 | Viewed by 5460

Abstract

Fourier transform infrared (FT-IR) and Raman spectroscopy and mapping were applied to the analysis of biofilms produced by bacteria of the genus Streptococcus. Bacterial biofilm, also called dental plaque, is the main cause of periodontal disease and tooth decay. It consists of a complex microbial community embedded in an extracellular matrix composed of highly hydrated extracellular polymeric substances and is a combination of salivary and bacterial proteins, lipids, polysaccharides, nucleic acids, and inorganic ions. This study confirms the value of Raman and FT-IR spectroscopies in biology, medicine, and pharmacy as effective tools for bacterial product characterization. Full article

(This article belongs to the Special Issue Bacterial Carbohydrates: Structures, Applications, and Structure/Activity Relationships)

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