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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doaj-6838d8b21e594204807225e828b2aa142020-11-25T04:10:02ZengMDPI AGLife2075-17292020-11-011028028010.3390/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 |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
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 |
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 |
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 |
title |
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_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_sort |
dual rnase and β-lactamase activity of a single enzyme encoded in archaea |
publisher |
MDPI AG |
series |
Life |
issn |
2075-1729 |
publishDate |
2020-11-01 |
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. |
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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