Dual RNase and β-lactamase Activity of a Single Enzyme Encoded in Archaea
β-lactam antibiotics have a well-known activity which disturbs the bacterial cell wall biosynthesis and may be cleaved by β-lactamases. However, these drugs are not active on archaea microorganisms, which are naturally resistant because of the lack of β-lactam target in their cell wall. Here, we des...
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| Format: | Article |
| Language: | English |
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MDPI AG
2020-11-01
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| Series: | Life |
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| Online Access: | https://www.mdpi.com/2075-1729/10/11/280 |
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| author | Seydina M. Diene Lucile Pinault Nicholas Armstrong Said Azza Vivek Keshri Saber Khelaifia Eric Chabrière Gustavo Caetano-Anolles Jean-Marc Rolain Pierre Pontarotti Didier Raoult |
| author_facet | Seydina M. Diene Lucile Pinault Nicholas Armstrong Said Azza Vivek Keshri Saber Khelaifia Eric Chabrière Gustavo Caetano-Anolles Jean-Marc Rolain Pierre Pontarotti Didier Raoult |
| author_sort | Seydina M. Diene |
| collection | DOAJ |
| description | β-lactam antibiotics have a well-known activity which disturbs the bacterial cell wall biosynthesis and may be cleaved by β-lactamases. However, these drugs are not active on archaea microorganisms, which are naturally resistant because of the lack of β-lactam target in their cell wall. Here, we describe that annotation of genes as β-lactamases in Archaea on the basis of homologous genes is a remnant of identification of the original activities of this group of enzymes, which in fact have multiple functions, including nuclease, ribonuclease, β-lactamase, or glyoxalase, which may specialized over time. We expressed class B β-lactamase enzyme from Methanosarcina barkeri that digest penicillin G. Moreover, while weak glyoxalase activity was detected, a significant ribonuclease activity on bacterial and synthetic RNAs was demonstrated. The β-lactamase activity was inhibited by β-lactamase inhibitor (sulbactam), but its RNAse activity was not. This gene appears to have been transferred to the Flavobacteriaceae group especially the Elizabethkingia genus, in which the expressed gene shows a more specialized activity on thienamycin, but no glyoxalase activity. The expressed class C-like β-lactamase gene, from Methanosarcina sp., also shows hydrolysis activity on nitrocefin and is more closely related to DD-peptidase enzymes. Our findings highlight the need to redefine the nomenclature of β-lactamase enzymes and the specification of multipotent enzymes in different ways in Archaea and bacteria over time. |
| first_indexed | 2024-03-10T14:50:50Z |
| format | Article |
| id | doaj.art-6838d8b21e594204807225e828b2aa14 |
| institution | Directory Open Access Journal |
| issn | 2075-1729 |
| language | English |
| last_indexed | 2024-03-10T14:50:50Z |
| publishDate | 2020-11-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Life |
| spelling | doaj.art-6838d8b21e594204807225e828b2aa142023-11-20T20:59:48ZengMDPI AGLife2075-17292020-11-01101128010.3390/life10110280Dual RNase and β-lactamase Activity of a Single Enzyme Encoded in ArchaeaSeydina M. Diene0Lucile Pinault1Nicholas Armstrong2Said Azza3Vivek Keshri4Saber Khelaifia5Eric Chabrière6Gustavo Caetano-Anolles7Jean-Marc Rolain8Pierre Pontarotti9Didier Raoult10MEPHI, IHU-Mediterranee Infection, Aix Marseille University, 19-21 Bd Jean Moulin, 13005 Marseille, FranceAssistance Publique-Hôpitaux de Marseille (AP-HM), IHU-Méditerranée Infection, 13005 Marseille, FranceAssistance Publique-Hôpitaux de Marseille (AP-HM), IHU-Méditerranée Infection, 13005 Marseille, FranceAssistance Publique-Hôpitaux de Marseille (AP-HM), IHU-Méditerranée Infection, 13005 Marseille, FranceMEPHI, IHU-Mediterranee Infection, Aix Marseille University, 19-21 Bd Jean Moulin, 13005 Marseille, FranceIHU-Méditerranée Infection, 13005 Marseille, FranceMEPHI, IHU-Mediterranee Infection, Aix Marseille University, 19-21 Bd Jean Moulin, 13005 Marseille, FranceEvolutionary Bioinformatics Laboratory, Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USAMEPHI, IHU-Mediterranee Infection, Aix Marseille University, 19-21 Bd Jean Moulin, 13005 Marseille, FranceMEPHI, IHU-Mediterranee Infection, Aix Marseille University, 19-21 Bd Jean Moulin, 13005 Marseille, FranceMEPHI, IHU-Mediterranee Infection, Aix Marseille University, 19-21 Bd Jean Moulin, 13005 Marseille, Franceβ-lactam antibiotics have a well-known activity which disturbs the bacterial cell wall biosynthesis and may be cleaved by β-lactamases. However, these drugs are not active on archaea microorganisms, which are naturally resistant because of the lack of β-lactam target in their cell wall. Here, we describe that annotation of genes as β-lactamases in Archaea on the basis of homologous genes is a remnant of identification of the original activities of this group of enzymes, which in fact have multiple functions, including nuclease, ribonuclease, β-lactamase, or glyoxalase, which may specialized over time. We expressed class B β-lactamase enzyme from Methanosarcina barkeri that digest penicillin G. Moreover, while weak glyoxalase activity was detected, a significant ribonuclease activity on bacterial and synthetic RNAs was demonstrated. The β-lactamase activity was inhibited by β-lactamase inhibitor (sulbactam), but its RNAse activity was not. This gene appears to have been transferred to the Flavobacteriaceae group especially the Elizabethkingia genus, in which the expressed gene shows a more specialized activity on thienamycin, but no glyoxalase activity. The expressed class C-like β-lactamase gene, from Methanosarcina sp., also shows hydrolysis activity on nitrocefin and is more closely related to DD-peptidase enzymes. Our findings highlight the need to redefine the nomenclature of β-lactamase enzymes and the specification of multipotent enzymes in different ways in Archaea and bacteria over time.https://www.mdpi.com/2075-1729/10/11/280archaeametallo-β-lactamasesribonucleasesglyoxalasescommon ancestor sequencecore genes |
| spellingShingle | Seydina M. Diene Lucile Pinault Nicholas Armstrong Said Azza Vivek Keshri Saber Khelaifia Eric Chabrière Gustavo Caetano-Anolles Jean-Marc Rolain Pierre Pontarotti Didier Raoult Dual RNase and β-lactamase Activity of a Single Enzyme Encoded in Archaea Life archaea metallo-β-lactamases ribonucleases glyoxalases common ancestor sequence core genes |
| title | Dual RNase and β-lactamase Activity of a Single Enzyme Encoded in Archaea |
| title_full | Dual RNase and β-lactamase Activity of a Single Enzyme Encoded in Archaea |
| title_fullStr | Dual RNase and β-lactamase Activity of a Single Enzyme Encoded in Archaea |
| title_full_unstemmed | Dual RNase and β-lactamase Activity of a Single Enzyme Encoded in Archaea |
| title_short | Dual RNase and β-lactamase Activity of a Single Enzyme Encoded in Archaea |
| title_sort | dual rnase and β lactamase activity of a single enzyme encoded in archaea |
| topic | archaea metallo-β-lactamases ribonucleases glyoxalases common ancestor sequence core genes |
| url | https://www.mdpi.com/2075-1729/10/11/280 |
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