Specialized acyl carrier protein used by serine palmitoyltransferase to synthesize sphingolipids in Rhodobacteria
Serine palmitoyltransferase (SPT) catalyzes the first and committed step in sphingolipid biosynthesis condensating L-serine and acyl-CoA to form 3-oxo-sphinganine. Whenever the structural gene for SPT is present in genomes of Rhodobacteria (α-, β-, and γ-Proteobacteria), it co-occurs with genes codi...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-08-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.961041/full |
| _version_ | 1818172652826656768 |
|---|---|
| author | Jonathan Padilla-Gómez Roberto Jhonatan Olea-Ozuna Sandra Contreras-Martínez Orlando Morales-Tarré Daniela A. García-Soriano Diana X. Sahonero-Canavesi Sebastian Poggio Sergio Encarnación-Guevara Isabel M. López-Lara Otto Geiger |
| author_facet | Jonathan Padilla-Gómez Roberto Jhonatan Olea-Ozuna Sandra Contreras-Martínez Orlando Morales-Tarré Daniela A. García-Soriano Diana X. Sahonero-Canavesi Sebastian Poggio Sergio Encarnación-Guevara Isabel M. López-Lara Otto Geiger |
| author_sort | Jonathan Padilla-Gómez |
| collection | DOAJ |
| description | Serine palmitoyltransferase (SPT) catalyzes the first and committed step in sphingolipid biosynthesis condensating L-serine and acyl-CoA to form 3-oxo-sphinganine. Whenever the structural gene for SPT is present in genomes of Rhodobacteria (α-, β-, and γ-Proteobacteria), it co-occurs with genes coding for a putative acyl carrier protein (ACP) and a putative acyl-CoA synthetase (ACS). In the α-proteobacterium Caulobacter crescentus, CC_1162 encodes an SPT, whereas CC_1163 and CC_1165 encode the putative ACP and ACS, respectively, and all three genes are known to be required for the formation of the sphingolipid intermediate 3-oxo-sphinganine. Here we show that the putative ACP possesses a 4'-phosphopantetheine prosthetic group, is selectively acylated by the putative ACS and therefore is a specialized ACP (AcpR) required for sphingolipid biosynthesis in Rhodobacteria. The putative ACS is unable to acylate coenzyme A or housekeeping ACPs, but acylates specifically AcpR. Therefore, it is a specialized acyl-ACP synthetase (AasR). SPTs from C. crescentus, Escherichia coli B, or Sphingomonas wittichii use preferentially acyl-AcpR as thioester substrate for 3-oxo-sphinganine synthesis. Whereas acyl-AcpR from C. crescentus is a good substrate for SPTs from distinct Rhodobacteria, acylation of a specific AcpR is achieved by the cognate AasR from the same bacterium. Rhodobacteria might use this more complex way of 3-oxo-sphinganine formation in order to direct free fatty acids toward sphingolipid biosynthesis. |
| first_indexed | 2024-12-11T19:16:01Z |
| format | Article |
| id | doaj.art-9fa27d28265b4f50840614714db5dd89 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-11T19:16:01Z |
| publishDate | 2022-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-9fa27d28265b4f50840614714db5dd892022-12-22T00:53:39ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-08-011310.3389/fmicb.2022.961041961041Specialized acyl carrier protein used by serine palmitoyltransferase to synthesize sphingolipids in RhodobacteriaJonathan Padilla-Gómez0Roberto Jhonatan Olea-Ozuna1Sandra Contreras-Martínez2Orlando Morales-Tarré3Daniela A. García-Soriano4Diana X. Sahonero-Canavesi5Sebastian Poggio6Sergio Encarnación-Guevara7Isabel M. López-Lara8Otto Geiger9Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, MexicoCentro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, MexicoCentro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, MexicoCentro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, MexicoCentro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, MexicoCentro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, MexicoInstituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Ciudad de México, MexicoCentro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, MexicoCentro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, MexicoCentro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, MexicoSerine palmitoyltransferase (SPT) catalyzes the first and committed step in sphingolipid biosynthesis condensating L-serine and acyl-CoA to form 3-oxo-sphinganine. Whenever the structural gene for SPT is present in genomes of Rhodobacteria (α-, β-, and γ-Proteobacteria), it co-occurs with genes coding for a putative acyl carrier protein (ACP) and a putative acyl-CoA synthetase (ACS). In the α-proteobacterium Caulobacter crescentus, CC_1162 encodes an SPT, whereas CC_1163 and CC_1165 encode the putative ACP and ACS, respectively, and all three genes are known to be required for the formation of the sphingolipid intermediate 3-oxo-sphinganine. Here we show that the putative ACP possesses a 4'-phosphopantetheine prosthetic group, is selectively acylated by the putative ACS and therefore is a specialized ACP (AcpR) required for sphingolipid biosynthesis in Rhodobacteria. The putative ACS is unable to acylate coenzyme A or housekeeping ACPs, but acylates specifically AcpR. Therefore, it is a specialized acyl-ACP synthetase (AasR). SPTs from C. crescentus, Escherichia coli B, or Sphingomonas wittichii use preferentially acyl-AcpR as thioester substrate for 3-oxo-sphinganine synthesis. Whereas acyl-AcpR from C. crescentus is a good substrate for SPTs from distinct Rhodobacteria, acylation of a specific AcpR is achieved by the cognate AasR from the same bacterium. Rhodobacteria might use this more complex way of 3-oxo-sphinganine formation in order to direct free fatty acids toward sphingolipid biosynthesis.https://www.frontiersin.org/articles/10.3389/fmicb.2022.961041/fullACPacyl-ACP synthetasefatty acid metabolismserine palmitoyltransferase3-oxo-sphinganinesphingolipid |
| spellingShingle | Jonathan Padilla-Gómez Roberto Jhonatan Olea-Ozuna Sandra Contreras-Martínez Orlando Morales-Tarré Daniela A. García-Soriano Diana X. Sahonero-Canavesi Sebastian Poggio Sergio Encarnación-Guevara Isabel M. López-Lara Otto Geiger Specialized acyl carrier protein used by serine palmitoyltransferase to synthesize sphingolipids in Rhodobacteria Frontiers in Microbiology ACP acyl-ACP synthetase fatty acid metabolism serine palmitoyltransferase 3-oxo-sphinganine sphingolipid |
| title | Specialized acyl carrier protein used by serine palmitoyltransferase to synthesize sphingolipids in Rhodobacteria |
| title_full | Specialized acyl carrier protein used by serine palmitoyltransferase to synthesize sphingolipids in Rhodobacteria |
| title_fullStr | Specialized acyl carrier protein used by serine palmitoyltransferase to synthesize sphingolipids in Rhodobacteria |
| title_full_unstemmed | Specialized acyl carrier protein used by serine palmitoyltransferase to synthesize sphingolipids in Rhodobacteria |
| title_short | Specialized acyl carrier protein used by serine palmitoyltransferase to synthesize sphingolipids in Rhodobacteria |
| title_sort | specialized acyl carrier protein used by serine palmitoyltransferase to synthesize sphingolipids in rhodobacteria |
| topic | ACP acyl-ACP synthetase fatty acid metabolism serine palmitoyltransferase 3-oxo-sphinganine sphingolipid |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.961041/full |
| work_keys_str_mv | AT jonathanpadillagomez specializedacylcarrierproteinusedbyserinepalmitoyltransferasetosynthesizesphingolipidsinrhodobacteria AT robertojhonatanoleaozuna specializedacylcarrierproteinusedbyserinepalmitoyltransferasetosynthesizesphingolipidsinrhodobacteria AT sandracontrerasmartinez specializedacylcarrierproteinusedbyserinepalmitoyltransferasetosynthesizesphingolipidsinrhodobacteria AT orlandomoralestarre specializedacylcarrierproteinusedbyserinepalmitoyltransferasetosynthesizesphingolipidsinrhodobacteria AT danielaagarciasoriano specializedacylcarrierproteinusedbyserinepalmitoyltransferasetosynthesizesphingolipidsinrhodobacteria AT dianaxsahonerocanavesi specializedacylcarrierproteinusedbyserinepalmitoyltransferasetosynthesizesphingolipidsinrhodobacteria AT sebastianpoggio specializedacylcarrierproteinusedbyserinepalmitoyltransferasetosynthesizesphingolipidsinrhodobacteria AT sergioencarnacionguevara specializedacylcarrierproteinusedbyserinepalmitoyltransferasetosynthesizesphingolipidsinrhodobacteria AT isabelmlopezlara specializedacylcarrierproteinusedbyserinepalmitoyltransferasetosynthesizesphingolipidsinrhodobacteria AT ottogeiger specializedacylcarrierproteinusedbyserinepalmitoyltransferasetosynthesizesphingolipidsinrhodobacteria |