Adaptation of the <i>Romanomermis culicivorax</i> CCA-Adding Enzyme to Miniaturized Armless tRNA Substrates
The mitochondrial genome of the nematode <i>Romanomermis culicivorax</i> encodes for miniaturized hairpin-like tRNA molecules that lack D- as well as T-arms, strongly deviating from the consensus cloverleaf. The single tRNA nucleotidyltransferase of this organism is fully active on armle...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2020-11-01
|
| Series: | International Journal of Molecular Sciences |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1422-0067/21/23/9047 |
| _version_ | 1797546412933644288 |
|---|---|
| author | Oliver Hennig Susanne Philipp Sonja Bonin Kévin Rollet Tim Kolberg Tina Jühling Heike Betat Claude Sauter Mario Mörl |
| author_facet | Oliver Hennig Susanne Philipp Sonja Bonin Kévin Rollet Tim Kolberg Tina Jühling Heike Betat Claude Sauter Mario Mörl |
| author_sort | Oliver Hennig |
| collection | DOAJ |
| description | The mitochondrial genome of the nematode <i>Romanomermis culicivorax</i> encodes for miniaturized hairpin-like tRNA molecules that lack D- as well as T-arms, strongly deviating from the consensus cloverleaf. The single tRNA nucleotidyltransferase of this organism is fully active on armless tRNAs, while the human counterpart is not able to add a complete CCA-end. Transplanting single regions of the <i>Romanomermis</i> enzyme into the human counterpart, we identified a beta-turn element of the catalytic core that—when inserted into the human enzyme—confers full CCA-adding activity on armless tRNAs. This region, originally identified to position the 3′-end of the tRNA primer in the catalytic core, dramatically increases the enzyme’s substrate affinity. While conventional tRNA substrates bind to the enzyme by interactions with the T-arm, this is not possible in the case of armless tRNAs, and the strong contribution of the beta-turn compensates for an otherwise too weak interaction required for the addition of a complete CCA-terminus. This compensation demonstrates the remarkable evolutionary plasticity of the catalytic core elements of this enzyme to adapt to unconventional tRNA substrates. |
| first_indexed | 2024-03-10T14:29:23Z |
| format | Article |
| id | doaj.art-ad6ce3309b18433cb2868dcbc8fefe3c |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T14:29:23Z |
| publishDate | 2020-11-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-ad6ce3309b18433cb2868dcbc8fefe3c2023-11-20T22:43:09ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-11-012123904710.3390/ijms21239047Adaptation of the <i>Romanomermis culicivorax</i> CCA-Adding Enzyme to Miniaturized Armless tRNA SubstratesOliver Hennig0Susanne Philipp1Sonja Bonin2Kévin Rollet3Tim Kolberg4Tina Jühling5Heike Betat6Claude Sauter7Mario Mörl8Institute for Biochemistry, Leipzig University, Brüderstraße 34, 04103 Leipzig, GermanyInstitute for Biochemistry, Leipzig University, Brüderstraße 34, 04103 Leipzig, GermanyInstitute for Biochemistry, Leipzig University, Brüderstraße 34, 04103 Leipzig, GermanyInstitute for Biochemistry, Leipzig University, Brüderstraße 34, 04103 Leipzig, GermanyInstitute for Biochemistry, Leipzig University, Brüderstraße 34, 04103 Leipzig, GermanyInstitute for Biochemistry, Leipzig University, Brüderstraße 34, 04103 Leipzig, GermanyInstitute for Biochemistry, Leipzig University, Brüderstraße 34, 04103 Leipzig, GermanyArchitecture et Réactivité de l’ARN, Université de Strasbourg, CNRS, IBMC, 67084 Strasbourg, FranceInstitute for Biochemistry, Leipzig University, Brüderstraße 34, 04103 Leipzig, GermanyThe mitochondrial genome of the nematode <i>Romanomermis culicivorax</i> encodes for miniaturized hairpin-like tRNA molecules that lack D- as well as T-arms, strongly deviating from the consensus cloverleaf. The single tRNA nucleotidyltransferase of this organism is fully active on armless tRNAs, while the human counterpart is not able to add a complete CCA-end. Transplanting single regions of the <i>Romanomermis</i> enzyme into the human counterpart, we identified a beta-turn element of the catalytic core that—when inserted into the human enzyme—confers full CCA-adding activity on armless tRNAs. This region, originally identified to position the 3′-end of the tRNA primer in the catalytic core, dramatically increases the enzyme’s substrate affinity. While conventional tRNA substrates bind to the enzyme by interactions with the T-arm, this is not possible in the case of armless tRNAs, and the strong contribution of the beta-turn compensates for an otherwise too weak interaction required for the addition of a complete CCA-terminus. This compensation demonstrates the remarkable evolutionary plasticity of the catalytic core elements of this enzyme to adapt to unconventional tRNA substrates.https://www.mdpi.com/1422-0067/21/23/9047CCA-adding enzymeco-evolutionevolutionary plasticityminimalized armless tRNAstRNA nucleotidyltransferase |
| spellingShingle | Oliver Hennig Susanne Philipp Sonja Bonin Kévin Rollet Tim Kolberg Tina Jühling Heike Betat Claude Sauter Mario Mörl Adaptation of the <i>Romanomermis culicivorax</i> CCA-Adding Enzyme to Miniaturized Armless tRNA Substrates International Journal of Molecular Sciences CCA-adding enzyme co-evolution evolutionary plasticity minimalized armless tRNAs tRNA nucleotidyltransferase |
| title | Adaptation of the <i>Romanomermis culicivorax</i> CCA-Adding Enzyme to Miniaturized Armless tRNA Substrates |
| title_full | Adaptation of the <i>Romanomermis culicivorax</i> CCA-Adding Enzyme to Miniaturized Armless tRNA Substrates |
| title_fullStr | Adaptation of the <i>Romanomermis culicivorax</i> CCA-Adding Enzyme to Miniaturized Armless tRNA Substrates |
| title_full_unstemmed | Adaptation of the <i>Romanomermis culicivorax</i> CCA-Adding Enzyme to Miniaturized Armless tRNA Substrates |
| title_short | Adaptation of the <i>Romanomermis culicivorax</i> CCA-Adding Enzyme to Miniaturized Armless tRNA Substrates |
| title_sort | adaptation of the i romanomermis culicivorax i cca adding enzyme to miniaturized armless trna substrates |
| topic | CCA-adding enzyme co-evolution evolutionary plasticity minimalized armless tRNAs tRNA nucleotidyltransferase |
| url | https://www.mdpi.com/1422-0067/21/23/9047 |
| work_keys_str_mv | AT oliverhennig adaptationoftheiromanomermisculicivoraxiccaaddingenzymetominiaturizedarmlesstrnasubstrates AT susannephilipp adaptationoftheiromanomermisculicivoraxiccaaddingenzymetominiaturizedarmlesstrnasubstrates AT sonjabonin adaptationoftheiromanomermisculicivoraxiccaaddingenzymetominiaturizedarmlesstrnasubstrates AT kevinrollet adaptationoftheiromanomermisculicivoraxiccaaddingenzymetominiaturizedarmlesstrnasubstrates AT timkolberg adaptationoftheiromanomermisculicivoraxiccaaddingenzymetominiaturizedarmlesstrnasubstrates AT tinajuhling adaptationoftheiromanomermisculicivoraxiccaaddingenzymetominiaturizedarmlesstrnasubstrates AT heikebetat adaptationoftheiromanomermisculicivoraxiccaaddingenzymetominiaturizedarmlesstrnasubstrates AT claudesauter adaptationoftheiromanomermisculicivoraxiccaaddingenzymetominiaturizedarmlesstrnasubstrates AT mariomorl adaptationoftheiromanomermisculicivoraxiccaaddingenzymetominiaturizedarmlesstrnasubstrates |