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

Zhaobin Huang,Jieqing Liu,Le Dong,Qiliang Lai

doi:10.3389/fmicb.2020.02056

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 S2-4-1HT, 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 S2-4-1HT 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 S2-4-1HT represented a novel genus-level species named Spartinivicinus ruber gen. nov., sp. nov. (type strain S2-4-1HT = MCCC 1K03745T = KCTC 72148T). Our study provided a novel bacterial source and novel prodigiosin analogs as promising pharmaceuticals in biotechnological application.

Highlights

Prodiginines are a large family of red pigments bearing the linear tripyrrole core structure, which are produced by bacteria as secondary metabolites (Hu et al, 2016)
Phylogenetic Analysis of Strain S2-4-1HT Based on 16S rRNA Gene
The sequence similarity search against the EzBioCloud database showed that it had maximum similarities of 93.4, 93.4, 93.2, and 92.5% with Z. ganghwensis JC2044T, Aestuariirhabdus litorea GTF13T, Z. marina JC333T, and Endozoicomonas euniceicola EF212T, respectively, indicating that strain S2-4-1HT represented a novel species, which was below the threshold for differentiating two species based on 16S rRNA gene sequence similarity of 98.65% (Kim et al, 2014)

Summary

INTRODUCTION

Prodiginines are a large family of red pigments bearing the linear tripyrrole core structure, which are produced by bacteria as secondary metabolites (Hu et al, 2016). Several gammaproteobacterial species, such as P. rubra (Gerber and Gauthier, 1979) and Z. marina (Ramaprasad et al, 2015), are reported to simultaneously produce prodigiosin (C20H25N3O) and its carbocyclic isoform, cycloprodigiosin (C20H23N3O) as major components. Heptylprodigiosin (a heptyl chain at C-3 position, C22H29N3O) has only been reported in a marine alphaproteobacterium, Pseudovibrio denitrificans, as a major component (Sertan-de Guzman et al, 2007) and in several marine gammaproteobacteria, Z. marina (Ramaprasad et al, 2015), Z. rubidus (Lee et al, 2011), and H. chejuensis (Kim et al, 2007), in minor amounts, whereas the chemical structure of its corresponding carbocyclic form is not reported so far. The biosynthesis of streptorubin B from undecylprodigiosin is accomplished by an enzyme named RedG in the red gene cluster of S. coelicolor A3(2). We determined the taxonomic position of strain S2-4-1HT using a polyphasic taxonomic approach

MATERIALS AND METHODS

RESULTS

DISCUSSION

DATA AVAILABILITY STATEMENT