Targeted disruption of the cls gene in Buchnera aphidicola impairs membrane integrity and host symbiont dynamics
Summary: The obligate symbiosis between pea aphids (Acyrthosiphon pisum) and Buchnera aphidicola represents metabolic interdependence between the host insect and its bacterial symbiont. Buchnera has a highly reduced genome that has lost nearly all phospholipid synthesis genes except cls, encoding a...
Saved in:
| Main Authors: | , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2025-08-01
|
| Series: | iScience |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004225014397 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850033619243892736 |
|---|---|
| author | Kathrine Xin Yee Tan Shuji Shigenobu |
| author_facet | Kathrine Xin Yee Tan Shuji Shigenobu |
| author_sort | Kathrine Xin Yee Tan |
| collection | DOAJ |
| description | Summary: The obligate symbiosis between pea aphids (Acyrthosiphon pisum) and Buchnera aphidicola represents metabolic interdependence between the host insect and its bacterial symbiont. Buchnera has a highly reduced genome that has lost nearly all phospholipid synthesis genes except cls, encoding a cardiolipin synthase homologue. We employed in vivo antisense, cell-penetrating peptide (CPP)-conjugated synthetic peptide nucleic acids (PNAs) to knock down cls in Buchnera. This intervention resulted in significant downregulation of cls expression, lowered Buchnera titers, pronounced morphological distortions, and reduced aphid reproduction. Notably, Buchnera cells were often detected in the aphid gut following anti-cls PNAs treatment, deviating from their typical intracellular niche within bacteriocytes. Collectively, the cls gene is critical for maintaining Buchnera integrity, proper cellular localization, and symbiont-host interactions. Given that the retention of cls is a common feature among many obligate endosymbionts despite massive gene loss, our findings offer key insights into the evolutionary principles shaping symbiotic relationships involving membrane biology. |
| format | Article |
| id | doaj-art-704b08ce832c4c8bb4352c5f786fdafd |
| institution | DOAJ |
| issn | 2589-0042 |
| language | English |
| publishDate | 2025-08-01 |
| publisher | Elsevier |
| record_format | Article |
| series | iScience |
| spelling | doaj-art-704b08ce832c4c8bb4352c5f786fdafd2025-08-20T02:58:08ZengElsevieriScience2589-00422025-08-0128811317810.1016/j.isci.2025.113178Targeted disruption of the cls gene in Buchnera aphidicola impairs membrane integrity and host symbiont dynamicsKathrine Xin Yee Tan0Shuji Shigenobu1Department of Basic Biology, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan; Laboratory of Evolutionary Genomics, National Institute for Basic Biology, Okazaki 444-8585, JapanDepartment of Basic Biology, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI), 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan; Laboratory of Evolutionary Genomics, National Institute for Basic Biology, Okazaki 444-8585, Japan; Life Science Center for Survival Dynamics, Tsukuba Advanced Research Alliance (TARA), University of Tsukuba, Tsukuba 305-8477, Japan; Corresponding authorSummary: The obligate symbiosis between pea aphids (Acyrthosiphon pisum) and Buchnera aphidicola represents metabolic interdependence between the host insect and its bacterial symbiont. Buchnera has a highly reduced genome that has lost nearly all phospholipid synthesis genes except cls, encoding a cardiolipin synthase homologue. We employed in vivo antisense, cell-penetrating peptide (CPP)-conjugated synthetic peptide nucleic acids (PNAs) to knock down cls in Buchnera. This intervention resulted in significant downregulation of cls expression, lowered Buchnera titers, pronounced morphological distortions, and reduced aphid reproduction. Notably, Buchnera cells were often detected in the aphid gut following anti-cls PNAs treatment, deviating from their typical intracellular niche within bacteriocytes. Collectively, the cls gene is critical for maintaining Buchnera integrity, proper cellular localization, and symbiont-host interactions. Given that the retention of cls is a common feature among many obligate endosymbionts despite massive gene loss, our findings offer key insights into the evolutionary principles shaping symbiotic relationships involving membrane biology.http://www.sciencedirect.com/science/article/pii/S2589004225014397Natural sciencesMicrobiologyBacteriologyEvolutionary biologyEvolutionary developmental biologyAgricultural science |
| spellingShingle | Kathrine Xin Yee Tan Shuji Shigenobu Targeted disruption of the cls gene in Buchnera aphidicola impairs membrane integrity and host symbiont dynamics iScience Natural sciences Microbiology Bacteriology Evolutionary biology Evolutionary developmental biology Agricultural science |
| title | Targeted disruption of the cls gene in Buchnera aphidicola impairs membrane integrity and host symbiont dynamics |
| title_full | Targeted disruption of the cls gene in Buchnera aphidicola impairs membrane integrity and host symbiont dynamics |
| title_fullStr | Targeted disruption of the cls gene in Buchnera aphidicola impairs membrane integrity and host symbiont dynamics |
| title_full_unstemmed | Targeted disruption of the cls gene in Buchnera aphidicola impairs membrane integrity and host symbiont dynamics |
| title_short | Targeted disruption of the cls gene in Buchnera aphidicola impairs membrane integrity and host symbiont dynamics |
| title_sort | targeted disruption of the cls gene in buchnera aphidicola impairs membrane integrity and host symbiont dynamics |
| topic | Natural sciences Microbiology Bacteriology Evolutionary biology Evolutionary developmental biology Agricultural science |
| url | http://www.sciencedirect.com/science/article/pii/S2589004225014397 |
| work_keys_str_mv | AT kathrinexinyeetan targeteddisruptionoftheclsgeneinbuchneraaphidicolaimpairsmembraneintegrityandhostsymbiontdynamics AT shujishigenobu targeteddisruptionoftheclsgeneinbuchneraaphidicolaimpairsmembraneintegrityandhostsymbiontdynamics |