Trans-4-hydroxy-L-proline catabolism by Pseudomonadota in the ocean

Free trans-4-hydroxy-L-proline (T4LHyp), a non-proteinogenic amino acid, is mainly released from the degradation of collagen, hydroxyproline-rich glycoproteins, and some peptide antibiotics in nature. Although it has been known that some terrestrial bacteria utilize T4LHyp as carbon and nitrogen source via a T4LHyp gene cluster, which and how marine microorganisms catabolize T4LHyp still remains unclear. Here, five T4LHyp-utilizing marine bacterial strains, Halomonas sp. 5021, Salinicola sp. 4072, Alteromonas sp. 6022, Alteromonas sp. 5112 and Alteromonas sp. 30521, were isolated from hydrothermal vent sediment samples collected from the southwest Indian Ocean. While Halomonas sp. 5021 can utilize T4LHyp as both a nitrogen and carbon source, the other four strains can utilize T4LHyp as only a nitrogen source. Then, the T4LHyp catabolic mechanisms of Halomonas sp. 5021 and Salinicola sp. 4072, as a representative of the four strains, were further investigated by genomic, transcriptional, and biochemical analyses. Halomonas sp. 5021 adopts an intact T4LHyp gene cluster containing four enzymes to catabolize T4LHyp into NH₃ and α-ketoglutarate to provide nitrogen and carbon sources for its growth. Compared to Halomonas sp. 5021, Salinicola sp. 4072 lacks an α-KGSA dehydrogenase gene in the T4LHyp gene cluster and can only catabolize T4LHyp into NH₃ and α-ketoglutarate semialdehyde to provide a nitrogen source for its growth. Bioinformatic investigation showed that the 5021-like and 4072-like T4LHyp gene clusters are predominantly found in bacteria from Pseudomonadota, which are widely distributed in multiple marine habitats. Thus, Pseudomonadota bacteria are likely the dominant group to drive the recycling and mineralization of T4LHyp in the ocean.

The online version contains supplementary material available at 10.1007/s42995-024-00272-8.