Membrane Vesicles Can Contribute to Cellulose Degradation by Teredinibacter turnerae, a Cultivable Intracellular Endosymbiont of Shipworms
ABSTRACT Teredinibacter turnerae is a cultivable cellulolytic Gammaproteobacterium (Cellvibrionaceae) that commonly occurs as an intracellular endosymbiont in the gills of wood‐eating bivalves of the family Teredinidae (shipworms). The genome of T. turnerae encodes a broad range of enzymes that deco...
Saved in:
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Wiley
2024-12-01
|
| Series: | Microbial Biotechnology |
| Subjects: | |
| Online Access: | https://doi.org/10.1111/1751-7915.70064 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850041499871346688 |
|---|---|
| author | Mark T. Gasser Annie Liu Marvin A. Altamia Bryan R. Brensinger Sarah L. Brewer Ron Flatau Eric R. Hancock Sarah P. Preheim Claire Marie Filone Daniel L. Distel |
| author_facet | Mark T. Gasser Annie Liu Marvin A. Altamia Bryan R. Brensinger Sarah L. Brewer Ron Flatau Eric R. Hancock Sarah P. Preheim Claire Marie Filone Daniel L. Distel |
| author_sort | Mark T. Gasser |
| collection | DOAJ |
| description | ABSTRACT Teredinibacter turnerae is a cultivable cellulolytic Gammaproteobacterium (Cellvibrionaceae) that commonly occurs as an intracellular endosymbiont in the gills of wood‐eating bivalves of the family Teredinidae (shipworms). The genome of T. turnerae encodes a broad range of enzymes that deconstruct cellulose, hemicellulose and pectin and contribute to wood (lignocellulose) digestion in the shipworm gut. However, the mechanisms by which T. turnerae secretes lignocellulolytic enzymes are incompletely understood. Here, we show that T. turnerae cultures grown on carboxymethyl cellulose (CMC) produce membrane vesicles (MVs) that include a variety of proteins identified by liquid chromatography–mass spectrometry (LC–MS/MS) as carbohydrate‐active enzymes (CAZymes) with predicted activities against cellulose, hemicellulose and pectin. Reducing sugar assays and zymography confirm that these MVs exhibit cellulolytic activity, as evidenced by the hydrolysis of CMC. Additionally, these MVs were enriched with TonB‐dependent receptors, which are essential to carbohydrate and iron acquisition by free‐living bacteria. These observations indicate a potential role for MVs in lignocellulose utilisation by T. turnerae in the free‐living state, suggest possible mechanisms for host–symbiont interaction and may be informative for commercial applications such as enzyme production and lignocellulosic biomass conversion. |
| format | Article |
| id | doaj-art-4e54a83dc9f245c0b0ff1acd8395bd6a |
| institution | DOAJ |
| issn | 1751-7915 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Wiley |
| record_format | Article |
| series | Microbial Biotechnology |
| spelling | doaj-art-4e54a83dc9f245c0b0ff1acd8395bd6a2025-08-20T02:55:46ZengWileyMicrobial Biotechnology1751-79152024-12-011712n/an/a10.1111/1751-7915.70064Membrane Vesicles Can Contribute to Cellulose Degradation by Teredinibacter turnerae, a Cultivable Intracellular Endosymbiont of ShipwormsMark T. Gasser0Annie Liu1Marvin A. Altamia2Bryan R. Brensinger3Sarah L. Brewer4Ron Flatau5Eric R. Hancock6Sarah P. Preheim7Claire Marie Filone8Daniel L. Distel9Johns Hopkins University Applied Physics Laboratory Laurel Maryland USAJohns Hopkins University Applied Physics Laboratory Laurel Maryland USAOcean Genome Legacy Center Northeastern University Nahant Massachusetts USAJohns Hopkins University Applied Physics Laboratory Laurel Maryland USAJohns Hopkins University Applied Physics Laboratory Laurel Maryland USAOcean Genome Legacy Center Northeastern University Nahant Massachusetts USAJohns Hopkins University Applied Physics Laboratory Laurel Maryland USAJohns Hopkins University Baltimore Maryland USAJohns Hopkins University Applied Physics Laboratory Laurel Maryland USAOcean Genome Legacy Center Northeastern University Nahant Massachusetts USAABSTRACT Teredinibacter turnerae is a cultivable cellulolytic Gammaproteobacterium (Cellvibrionaceae) that commonly occurs as an intracellular endosymbiont in the gills of wood‐eating bivalves of the family Teredinidae (shipworms). The genome of T. turnerae encodes a broad range of enzymes that deconstruct cellulose, hemicellulose and pectin and contribute to wood (lignocellulose) digestion in the shipworm gut. However, the mechanisms by which T. turnerae secretes lignocellulolytic enzymes are incompletely understood. Here, we show that T. turnerae cultures grown on carboxymethyl cellulose (CMC) produce membrane vesicles (MVs) that include a variety of proteins identified by liquid chromatography–mass spectrometry (LC–MS/MS) as carbohydrate‐active enzymes (CAZymes) with predicted activities against cellulose, hemicellulose and pectin. Reducing sugar assays and zymography confirm that these MVs exhibit cellulolytic activity, as evidenced by the hydrolysis of CMC. Additionally, these MVs were enriched with TonB‐dependent receptors, which are essential to carbohydrate and iron acquisition by free‐living bacteria. These observations indicate a potential role for MVs in lignocellulose utilisation by T. turnerae in the free‐living state, suggest possible mechanisms for host–symbiont interaction and may be informative for commercial applications such as enzyme production and lignocellulosic biomass conversion.https://doi.org/10.1111/1751-7915.70064carbohydrate‐active enzymesCAZymeslignocellulose degradationOMVsouter membrane vesiclessymbiosis |
| spellingShingle | Mark T. Gasser Annie Liu Marvin A. Altamia Bryan R. Brensinger Sarah L. Brewer Ron Flatau Eric R. Hancock Sarah P. Preheim Claire Marie Filone Daniel L. Distel Membrane Vesicles Can Contribute to Cellulose Degradation by Teredinibacter turnerae, a Cultivable Intracellular Endosymbiont of Shipworms Microbial Biotechnology carbohydrate‐active enzymes CAZymes lignocellulose degradation OMVs outer membrane vesicles symbiosis |
| title | Membrane Vesicles Can Contribute to Cellulose Degradation by Teredinibacter turnerae, a Cultivable Intracellular Endosymbiont of Shipworms |
| title_full | Membrane Vesicles Can Contribute to Cellulose Degradation by Teredinibacter turnerae, a Cultivable Intracellular Endosymbiont of Shipworms |
| title_fullStr | Membrane Vesicles Can Contribute to Cellulose Degradation by Teredinibacter turnerae, a Cultivable Intracellular Endosymbiont of Shipworms |
| title_full_unstemmed | Membrane Vesicles Can Contribute to Cellulose Degradation by Teredinibacter turnerae, a Cultivable Intracellular Endosymbiont of Shipworms |
| title_short | Membrane Vesicles Can Contribute to Cellulose Degradation by Teredinibacter turnerae, a Cultivable Intracellular Endosymbiont of Shipworms |
| title_sort | membrane vesicles can contribute to cellulose degradation by teredinibacter turnerae a cultivable intracellular endosymbiont of shipworms |
| topic | carbohydrate‐active enzymes CAZymes lignocellulose degradation OMVs outer membrane vesicles symbiosis |
| url | https://doi.org/10.1111/1751-7915.70064 |
| work_keys_str_mv | AT marktgasser membranevesiclescancontributetocellulosedegradationbyteredinibacterturneraeacultivableintracellularendosymbiontofshipworms AT annieliu membranevesiclescancontributetocellulosedegradationbyteredinibacterturneraeacultivableintracellularendosymbiontofshipworms AT marvinaaltamia membranevesiclescancontributetocellulosedegradationbyteredinibacterturneraeacultivableintracellularendosymbiontofshipworms AT bryanrbrensinger membranevesiclescancontributetocellulosedegradationbyteredinibacterturneraeacultivableintracellularendosymbiontofshipworms AT sarahlbrewer membranevesiclescancontributetocellulosedegradationbyteredinibacterturneraeacultivableintracellularendosymbiontofshipworms AT ronflatau membranevesiclescancontributetocellulosedegradationbyteredinibacterturneraeacultivableintracellularendosymbiontofshipworms AT ericrhancock membranevesiclescancontributetocellulosedegradationbyteredinibacterturneraeacultivableintracellularendosymbiontofshipworms AT sarahppreheim membranevesiclescancontributetocellulosedegradationbyteredinibacterturneraeacultivableintracellularendosymbiontofshipworms AT clairemariefilone membranevesiclescancontributetocellulosedegradationbyteredinibacterturneraeacultivableintracellularendosymbiontofshipworms AT danielldistel membranevesiclescancontributetocellulosedegradationbyteredinibacterturneraeacultivableintracellularendosymbiontofshipworms |