Recombineering enables genome mining of novel siderophores in a non-model Burkholderiales strain
Iron is essential for bacterial survival, and most bacteria capture iron by producing siderophores. Burkholderiales bacteria produce various types of bioactive secondary metabolites, such as ornibactin and malleobactin siderophores. In this study, the genome analysis of Burkholderiales genomes showe...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2023-09-01
|
| Series: | Engineering Microbiology |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2667370323000383 |
| _version_ | 1797671379555844096 |
|---|---|
| author | Xingyan Wang Haibo Zhou Xiangmei Ren Hanna Chen Lin Zhong Xianping Bai Xiaoying Bian |
| author_facet | Xingyan Wang Haibo Zhou Xiangmei Ren Hanna Chen Lin Zhong Xianping Bai Xiaoying Bian |
| author_sort | Xingyan Wang |
| collection | DOAJ |
| description | Iron is essential for bacterial survival, and most bacteria capture iron by producing siderophores. Burkholderiales bacteria produce various types of bioactive secondary metabolites, such as ornibactin and malleobactin siderophores. In this study, the genome analysis of Burkholderiales genomes showed a putative novel siderophore gene cluster crb, which is highly similar to the ornibactin and malleobactin gene clusters but does not have pvdF, a gene encoding a formyltransferase for N-δ‑hydroxy-ornithine formylation. Establishing the bacteriophage recombinase Redγ-Redαβ7029 mediated genome editing system in a non-model Burkholderiales strain Paraburkholderia caribensis CICC 10960 allowed the rapid identification of the products of crb gene cluster, caribactins A-F (1–6). Caribactins contain a special amino acid residue N-δ‑hydroxy-N-δ-acetylornithine (haOrn), which differs from the counterpart N-δ‑hydroxy-N-δ-formylornithine (hfOrn) in ornibactin and malleobactin, owing to the absence of pvdF. Gene inactivation showed that the acetylation of hOrn is catalyzed by CrbK, whose homologs probably not be involved in the biosynthesis of ornibactin and malleobactin, showing possible evolutionary clues of these siderophore biosynthetic pathways from different genera. Caribactins promote biofilm production and enhance swarming and swimming abilities, suggesting that they may play crucial roles in biofilm formation. This study also revealed that recombineering has the capability to mine novel secondary metabolites from non-model Burkholderiales species. |
| first_indexed | 2024-03-11T21:14:35Z |
| format | Article |
| id | doaj.art-1f148a5acd824512acb0b9e36398e063 |
| institution | Directory Open Access Journal |
| issn | 2667-3703 |
| language | English |
| last_indexed | 2024-03-11T21:14:35Z |
| publishDate | 2023-09-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Engineering Microbiology |
| spelling | doaj.art-1f148a5acd824512acb0b9e36398e0632023-09-29T04:45:31ZengElsevierEngineering Microbiology2667-37032023-09-0133100106Recombineering enables genome mining of novel siderophores in a non-model Burkholderiales strainXingyan Wang0Haibo Zhou1Xiangmei Ren2Hanna Chen3Lin Zhong4Xianping Bai5Xiaoying Bian6Helmholtz International Lab for Anti-Infectives, State Key Laboratory of Microbial Technology, Shandong University–Helmholtz Institute of Biotechnology, Shandong University, Qingdao 266237, ChinaHelmholtz International Lab for Anti-Infectives, State Key Laboratory of Microbial Technology, Shandong University–Helmholtz Institute of Biotechnology, Shandong University, Qingdao 266237, ChinaHelmholtz International Lab for Anti-Infectives, State Key Laboratory of Microbial Technology, Shandong University–Helmholtz Institute of Biotechnology, Shandong University, Qingdao 266237, ChinaHelmholtz International Lab for Anti-Infectives, State Key Laboratory of Microbial Technology, Shandong University–Helmholtz Institute of Biotechnology, Shandong University, Qingdao 266237, ChinaHelmholtz International Lab for Anti-Infectives, State Key Laboratory of Microbial Technology, Shandong University–Helmholtz Institute of Biotechnology, Shandong University, Qingdao 266237, ChinaHelmholtz International Lab for Anti-Infectives, State Key Laboratory of Microbial Technology, Shandong University–Helmholtz Institute of Biotechnology, Shandong University, Qingdao 266237, ChinaCorresponding author.; Helmholtz International Lab for Anti-Infectives, State Key Laboratory of Microbial Technology, Shandong University–Helmholtz Institute of Biotechnology, Shandong University, Qingdao 266237, ChinaIron is essential for bacterial survival, and most bacteria capture iron by producing siderophores. Burkholderiales bacteria produce various types of bioactive secondary metabolites, such as ornibactin and malleobactin siderophores. In this study, the genome analysis of Burkholderiales genomes showed a putative novel siderophore gene cluster crb, which is highly similar to the ornibactin and malleobactin gene clusters but does not have pvdF, a gene encoding a formyltransferase for N-δ‑hydroxy-ornithine formylation. Establishing the bacteriophage recombinase Redγ-Redαβ7029 mediated genome editing system in a non-model Burkholderiales strain Paraburkholderia caribensis CICC 10960 allowed the rapid identification of the products of crb gene cluster, caribactins A-F (1–6). Caribactins contain a special amino acid residue N-δ‑hydroxy-N-δ-acetylornithine (haOrn), which differs from the counterpart N-δ‑hydroxy-N-δ-formylornithine (hfOrn) in ornibactin and malleobactin, owing to the absence of pvdF. Gene inactivation showed that the acetylation of hOrn is catalyzed by CrbK, whose homologs probably not be involved in the biosynthesis of ornibactin and malleobactin, showing possible evolutionary clues of these siderophore biosynthetic pathways from different genera. Caribactins promote biofilm production and enhance swarming and swimming abilities, suggesting that they may play crucial roles in biofilm formation. This study also revealed that recombineering has the capability to mine novel secondary metabolites from non-model Burkholderiales species.http://www.sciencedirect.com/science/article/pii/S2667370323000383BurkholderialesRecombineeringSiderophoreGenome miningCaribactins |
| spellingShingle | Xingyan Wang Haibo Zhou Xiangmei Ren Hanna Chen Lin Zhong Xianping Bai Xiaoying Bian Recombineering enables genome mining of novel siderophores in a non-model Burkholderiales strain Engineering Microbiology Burkholderiales Recombineering Siderophore Genome mining Caribactins |
| title | Recombineering enables genome mining of novel siderophores in a non-model Burkholderiales strain |
| title_full | Recombineering enables genome mining of novel siderophores in a non-model Burkholderiales strain |
| title_fullStr | Recombineering enables genome mining of novel siderophores in a non-model Burkholderiales strain |
| title_full_unstemmed | Recombineering enables genome mining of novel siderophores in a non-model Burkholderiales strain |
| title_short | Recombineering enables genome mining of novel siderophores in a non-model Burkholderiales strain |
| title_sort | recombineering enables genome mining of novel siderophores in a non model burkholderiales strain |
| topic | Burkholderiales Recombineering Siderophore Genome mining Caribactins |
| url | http://www.sciencedirect.com/science/article/pii/S2667370323000383 |
| work_keys_str_mv | AT xingyanwang recombineeringenablesgenomeminingofnovelsiderophoresinanonmodelburkholderialesstrain AT haibozhou recombineeringenablesgenomeminingofnovelsiderophoresinanonmodelburkholderialesstrain AT xiangmeiren recombineeringenablesgenomeminingofnovelsiderophoresinanonmodelburkholderialesstrain AT hannachen recombineeringenablesgenomeminingofnovelsiderophoresinanonmodelburkholderialesstrain AT linzhong recombineeringenablesgenomeminingofnovelsiderophoresinanonmodelburkholderialesstrain AT xianpingbai recombineeringenablesgenomeminingofnovelsiderophoresinanonmodelburkholderialesstrain AT xiaoyingbian recombineeringenablesgenomeminingofnovelsiderophoresinanonmodelburkholderialesstrain |