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Spartinivicinus ruber gen. nov., sp. nov., a Novel Marine Gammaproteobacterium Producing Heptylprodigiosin and Cycloheptylprodigiosin as Major Red Pigments.

ABSTRACT: The red pigment prodiginines are identified as bacterial secondary metabolites and display a wide range of bioactive properties. Here, a novel rose-red pigmented bacterium, designated strain S2-4-1H^T, was isolated from coastal sediment of cordgrass Spartina alterniflora. Interestingly, it simultaneously produced heptylprodigiosin (C₂₂H₂₉N₃O) and cycloheptylprodigiosin (C₂₂H₂₇N₃O) as major red pigments, of which their chemical structures were established by liquid chromatography-mass spectrometry (LC-MS) and nuclear magnetic resonance (NMR). Bioactive assays revealed that both heptylprodigiosin and cycloheptylprodigiosin had antibacterial and antifungal activities, and notably, cycloheptylprodigiosin showed stronger bioactivity than heptylprodigiosin. The complete genome of strain S2-4-1H^T was determined to be 6,687,090 bp in length with a G + C content of 40.13 mol%, including a circular chromosome with a size of 6,361,125 bp and three plasmids with a size of 141,078, 102,423, and 82,464 bp, respectively. The biosynthetic gene cluster of two red pigments was predicted on a ∼41-kb gene fragment organized on the chromosome and displayed highly conserved features compared to several gammaproteobacterial species encoding the homologous genes. Finally, based on phenotypic, genotypic, and chemotaxonomic characteristics, strain S2-4-1H^T represented a novel genus-level species named Spartinivicinus ruber gen. nov., sp. nov. (type strain S2-4-1H^T = MCCC 1K03745^T = KCTC 72148^T). Our study provided a novel bacterial source and novel prodigiosin analogs as promising pharmaceuticals in biotechnological application.

SUBMITTER: Huang Z

PROVIDER: S-EPMC7484904 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: There is accumulating evidence that in some marine environments aerobic bacteriochlorophyll a-producing bacteria represent a significant part of the microbial population. The interaction of photosynthesis and carbon metabolism in these interesting bacteria is still largely unknown and requires further investigation in order to estimate their contribution to the marine carbon cycle. METHODOLOGY/PRINCIPAL FINDINGS: Here, we analyzed the structure, composition and regulation of the photosynthetic apparatus in the obligately aerobic marine gammaproteobacterium KT71(T). Photoheterotrophically grown cells were characterized by a poorly developed lamellar intracytoplasmic membrane system, a type 1 light-harvesting antenna complex and a photosynthetic reaction center associated with a tetraheme cytochrome c. The only photosynthetic pigments produced were bacteriochlorophyll a and spirilloxanthin. Under semiaerobic conditions KT71(T) cells expressing a photosynthetic apparatus showed a light-dependent increase of growth yield in the range of 1.3-2.5 fold. The expression level of the photosynthetic apparatus depended largely on the utilized substrate, the intermediary carbon metabolism and oxygen tension. In addition, pigment synthesis was strongly influenced by light, with blue light exerting the most significant effect, implicating that proteins containing a BLUF domain may be involved in regulation of the photosynthetic apparatus. Several phenotypic traits in KT71(T) could be identified that correlated with the assumed redox state of growing cells and thus could be used to monitor the cellular redox state under various incubation conditions. CONCLUSIONS/SIGNIFICANCE: In a hypothetical model that explains the regulation of the photosynthetic apparatus in strain KT71(T) we propose that the expression of photosynthesis genes depends on the cellular redox state and is maximal under conditions that allow a balanced membrane redox state. So far, bacteria capable of an obligately aerobic, photosynthetic metabolism constitute a unique phenotype within the class Gammaproteobacteria, so that it is justified to propose a new genus and species, Congregibacter litoralis gen. nov, sp. nov., represented by the type strain KT71(T) ( = DSM 17192(T) = NBRC 104960(T)).

Project description:Bacteria of the family Geobacteraceae are particularly common and deeply involved in many biogeochemical processes in terrestrial and freshwater environments. As part of a study to understand biogeochemical cycling in freshwater sediments, three iron-reducing isolates, designated as Red96T, Red100T, and Red88T, were isolated from the soils of two paddy fields and pond sediment located in Japan. The cells were Gram-negative, strictly anaerobic, rod-shaped, motile, and red-pigmented on agar plates. Growth of these three strains was coupled to the reduction of Fe(III)-NTA, Fe(III) citrate, and ferrihydrite with malate, methanol, pyruvate, and various organic acids and sugars serving as alternate electron donors. Phylogenetic analysis based on the housekeeping genes (16S rRNA gene, gyrB, rpoB, nifD, fusA, and recA) and 92 concatenated core genes indicated that all the isolates constituted a coherent cluster within the family Geobacteraceae. Genomic analyses, including average nucleotide identity and DNA-DNA hybridization, clearly differentiated the strains Red96T, Red100T, and Red88T from other species in the family Geobacteraceae, with values below the thresholds for species delineation. Along with the genomic comparison, the chemotaxonomic features further helped distinguish the three isolates from each other. In addition, the lower values of average amino acid identity and percentage of conserved protein, as well as biochemical differences with their relatives, indicated that the three strains represented a novel genus in the family Geobacteraceae. Hence, we concluded that strains Red96T, Red100T, and Red88T represented three novel species of a novel genus in the family Geobacteraceae, for which the names Oryzomonas japonicum gen. nov., sp. nov., Oryzomonas sagensis sp. nov., and Oryzomonas ruber sp. nov. are proposed, with type strains Red96T (= NBRC 114286T = MCCC 1K04376T), Red100T (= NBRC 114287T = MCCC 1K04377T), and Red88T (= MCCC 1K03694T = JCM 33033T), respectively.

Project description:Four novel strains were isolated: PWU4T and PWU20T were both from soil in Germany, PWU5T was isolated from soil in India and PWU37T was obtained from sheep faeces collected on the Island of Crete. Cells of each were observed to be Gram-negative, strictly aerobic, rod shaped, and to grow optimally between 28 and 34 °C, between pH 7.0 and 8.0 and without the addition of NaCl. The strains were found to be catalase and oxidase-negative and able to grow on most mono- and disaccharides, a few polysaccharides and organic acids. Their predominant menaquinone was identified as MK-7. Their major fatty acids were identified as C16:1 ω7c (PWU4T and PWU20T) and C16:1 ω5c (PWU5T and PWU37T). The DNA G + C contents of strains PWU4T, PWU20T, PWU5T and PWU37T were determined to be 50.2 mol%, 51.6 mol %, 39.8 mol% and 53.8 mol%, respectively. The 16S rRNA gene sequence analysis revealed that the close relatives Ohtaekwangia koreensis 3B-2T and Ohtaekwangia kribbensis 10AOT share less than 93.8% sequence similarity. The strains were classified in two groups, where PWU4T and PWU20T share 93.0% sequence similarity, and PWU5T and PWU37T share 97.5% sequence similarity. However, the members of each group were concluded to represent different species based on the low average nucleotide identity (ANI) of their genomes, 69.7% and 83.8%, respectively. We propose that the four strains represent four novel species of two new genera in the family Cytophagaceae. The type species of the novel genus Chryseosolibacter is Chryseosolibacter histidini gen. nov., sp. nov. with the type strain PWU4T (= DSM 111594T = NCCB 100798T), whilst strain PWU20T (= DSM 111597T = NCCB 100800T) is the type strain of a second species, Chryseosolibacter indicus sp. nov. The type species of the novel genus Dawidia is Dawidia cretensis gen. nov., sp. nov. with the type strain PWU5T (= DSM 111596T = NCCB 100799T), whilst strain PWU37T (= DSM 111595T = NCCB 100801T) is the type stain of a second species, Dawidia soli sp. nov.

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Spartinivicinus ruber gen. nov., sp. nov., a Novel Marine Gammaproteobacterium Producing Heptylprodigiosin and Cycloheptylprodigiosin as Major Red Pigments.

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