Identification and characterization of the α-CA in the outer membrane vesicles produced by  Helicobacter pylori

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Abstract

The genome of Helicobacter pylori encodes for carbonic anhydrases (CAs, EC 4.2.1.1) belonging to the α- and β-CA classes, which together with urease, have a pivotal role in the acid acclimation of the microorganism within the human stomach. Recently, in the exoproteome of H. pylori, a CA with no indication of the corresponding class was identified. Here, using the protonography and the mass spectrometry, a CA belonging to the α-class was detected in the outer membrane vesicles (OMVs) generated by planktonic and biofilm phenotypes of four H. pylori strains. The amount of this metalloenzyme was higher in the planktonic OMVs (pOMVs) than in the biofilm OMVs (bOMVs). Furthermore, the content of α-CA increases over time in the pOMVs. The identification of the α-CA in pOMVs and bOMVs might shed new light on the role of this enzyme in the colonization, survival, persistence, and pathogenesis of H. pylori.

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An overview of the alpha-, beta- and gamma-carbonic anhydrases from Bacteria: can bacterial carbonic anhydrases shed new light on evolution of bacteria?

Clemente Capasso, Claudiu Supuran (2015)

Carbonic anhydrases (CAs, EC 4.2.1.1) are metalloenzymes which catalyze a simple but physiologically crucial reaction in all life Domains, the carbon dioxide hydration to bicarbonate and protons: CO2 + H2O ⇔ HCO3(-)+ H(+). These enzymes are involved in many physiologic processes, such as photosynthesis, respiration, CO2 transport, as well as metabolism of xenobiotics. Five different, genetically distinct CA families are known to date: the α-, β-, γ-, δ- and ζ-CAs. α-, β- and δ-CAs use Zn(II) ions at the active site, the γ-CAs are probably Fe(II) enzymes (but they are active also with bound Zn(II) or Co(II) ions), whereas the ζ-class uses Cd(II) or Zn(II) to perform the physiologic reaction catalysis. Bacteria encode for enzymes belonging to the α-, β-, and γ-CA classes. They contain zinc ion (Zn(2+)) in their active site, coordinated by three histidine residues and a water molecule/hydroxide ion (in the α and γ) or by two cysteine and one histidine residues (in the β class), with the fourth ligand being a water molecule/hydroxide ion. Here we propose that bacterial CAs can be used as markers for understanding the evolution and genetic variability of the Gram-positive and Gram-negative bacteria. We addressed several questions such as: (1) why are α-CAs present only in the genome of Gram-negative bacteria; (2) why are α-CAs not present in all Gram-negative bacteria; (3) why do Bacteria show an intricate pattern of CA gene expression; (4) what are the physiologic roles of such diverse CAs in these prokaryotes. We proposed possible answers to the previous questions. Moreover, we speculated on the evolution of the CA classes (α, β and γ) identified in the Gram-negative and -positive bacteria. Our main hypothesis is that from the ancestral Ur-CA, the γ-class arose first, followed by the β-class; the α-class CAs came last it is found only in the Gram-negative bacteria.

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Mechanisms and Regulation of Extracellular DNA Release and Its Biological Roles in Microbial Communities

Alejandra L. Ibáñez de Aldecoa, Olga Zafra, José Gonzalez-Pastor (2017)

The capacity to release genetic material into the extracellular medium has been reported in cultures of numerous species of bacteria, archaea, and fungi, and also in the context of multicellular microbial communities such as biofilms. Moreover, extracellular DNA (eDNA) of microbial origin is widespread in natural aquatic and terrestrial environments. Different specific mechanisms are involved in eDNA release, such as autolysis and active secretion, as well as through its association with membrane vesicles. It is noteworthy that in microorganisms, in which DNA release has been studied in detail, the production of eDNA is coordinated by the population when it reaches a certain cell density, and is induced in a subpopulation in response to the accumulation of quorum sensing signals. Interestingly, in several bacteria there is also a relationship between eDNA release and the development of natural competence (the ability to take up DNA from the environment), which is also controlled by quorum sensing. Then, what is the biological function of eDNA? A common biological role has not been proposed, since different functions have been reported depending on the microorganism. However, it seems to be important in biofilm formation, can be used as a nutrient source, and could be involved in DNA damage repair and gene transfer. This review covers several aspects of eDNA research: (i) its occurrence and distribution in natural environments, (ii) the mechanisms and regulation of its release in cultured microorganisms, and (iii) its biological roles. In addition, we propose that eDNA release could be considered a social behavior, based on its quorum sensing-dependent regulation and on the described functions of eDNA in the context of microbial communities.

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Outer Membrane Vesicles of Helicobacter pylori TK1402 are Involved in Biofilm Formation

Hideo Yonezawa, Takako Osaki, Satoshi Kurata … (2009)

Background Helicobacter pylori forms biofilms on glass surfaces at the air-liquid interface in in vitro batch cultures; however, biofilms of H. pylori have not been well characterized. In the present study, we analyzed the ability of H. pylori strains to form biofilms and characterized the underlying mechanisms of H. pylori biofilm formation. Results Strain TK1402 showed strong biofilm forming ability relative to the other strains in Brucella broth supplemented with 7% FCS. The strong biofilm forming ability of TK1402 is reflected the relative thickness of the biofilms. In addition, outer membrane vesicles (OMV) were detected within the matrix of only the TK1402 biofilms. Biofilm formation was strongly correlated with the production of OMV in this strain. We further observed that strain TK1402 did not form thick biofilms in Brucella broth supplemented with 0.2% β-cyclodextrin. However, the addition of the OMV-fraction collected from TK1402 could enhance biofilm formation. Conclusion The results suggested that OMV produced from TK1402 play an important role in biofilm formation in strain TK1402.

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Author and article information

Journal

Journal ID (nlm-ta): J Enzyme Inhib Med Chem

Journal ID (iso-abbrev): J Enzyme Inhib Med Chem

Journal ID (publisher-id): IENZ

Journal ID (publisher-id): ienz20

Title: Journal of Enzyme Inhibition and Medicinal Chemistry

Publisher: Taylor & Francis

ISSN (Print): 1475-6366

ISSN (Electronic): 1475-6374

Publication date Collection: 2019

Publication date (Electronic): 07 January 2019

Volume: 34

Issue: 1

Pages: 189-195

Affiliations

[a ]CeSI-MeT Centro Scienze dell’Invecchiamento e Medicina Traslazionale, Center of Aging Sciences and Translational Medicine (CeSi-Met) , Chieti, Italy;

[b ]Department of Medical, Oral, and Biotechnological Sciences, University G. d’Annunzio of Chieti-Pescara , Chieti, Italy;

[c ]CNR, Istituto di Bioscienze e Biorisorse , Napoli, Italy;

[d ]Department of Medicine and Aging Science, G. d’Annunzio of Chieti-Pescara , Chieti, Italy;

[e ]Department of Pharmacy, University “G. d’Annunzio” of Chieti-Pescara , Chieti, Italy;

[f ]Dipartimento di Scienze Biomediche, Chirurgiche ed Odontoiatriche, University of Milan , Milan, Italy;

[g ]NEUROFARBA Department, Sezione di Scienze Farmaceutiche e Nutraceutiche, Università degli Studi di Firenze , Sesto, Italy

Author notes

[†]

These authors contributed equally.

CONTACT Rossella Grande rossella.grande@ 123456unich.it CeSI-MeT Centro Scienze dell’Invecchiamento e Medicina Traslazionale, Center of Aging Sciences and Translational Medicine (CeSi-Met) , Chieti, Italy;

Clemente Capasso clemente.capasso@ 123456ibbr.cnr.it CNR, Istituto di Bioscienze e Biorisorse , Napoli, Italy

Author information

Maurizio Ronci http://orcid.org/0000-0002-0797-6087

Francesca Sisto http://orcid.org/0000-0003-0166-2164

Claudiu T. Supuran http://orcid.org/0000-0003-4262-0323

Clemente Capasso http://orcid.org/0000-0003-3314-2411

Article

Publisher ID: 1539716

DOI: 10.1080/14756366.2018.1539716

PMC ID: 6327981

PubMed ID: 30734607

SO-VID: 4a044a36-882d-450e-8118-21b1cb11e1c8

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

History

Date received : 24 September 2018

Date accepted : 18 October 2018

Page count

Figures: 6, Tables: 1, Pages: 7, Words: 5282

Funding

Funded by: Ministero Italiano dell’Università e della Ricerca (MIUR) 10.13039/501100003407

This work was supported by Ministero Italiano dell’Università e della Ricerca (MIUR) FAR 2017 Grant held by Dr. Rossella Grande.

Identification and characterization of the α-CA in the outer membrane vesicles produced by Helicobacter pylori

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Most cited references 37

An overview of the alpha-, beta- and gamma-carbonic anhydrases from Bacteria: can bacterial carbonic anhydrases shed new light on evolution of bacteria?

Mechanisms and Regulation of Extracellular DNA Release and Its Biological Roles in Microbial Communities

Outer Membrane Vesicles of Helicobacter pylori TK1402 are Involved in Biofilm Formation

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