Genomic and physiological traits provide insights into ecological niche adaptations of mangrove endophytic Streptomyces parvulus VCCM 22513

Abstract

Abstract Purpose Endophytic Streptomyces parvulus VCCM 22513 isolated from Bruguiera gymnorrhiza in Quang Ninh mangrove forest, northern Vietnam showed abiotic stress tolerance consisting of antioxidant, salt-tolerant, and aromatic-compound degrading activities. The goal of this study was to shed light on genomic bases rendering mangrove endophytic S. parvulus more resilient to environmental stressors. Methods Phenotypic analysis including antioxidant activities, hydrogen peroxide and sodium chloride resistance, and aromatic compound utilization were evaluated. The genome of strain VCCM 22513 was sequenced using Illumina Miseq sequencing platform and assembled using SPAdes. Results Out of 15 endophytic actinomycetes associated with B. gymnorrhiza in Quang Ninh mangrove, northern Vietnam, VCCM 22513 extract showed remarkable antioxidant activities through (1,1-diphenyl-2-picrylhydrazyl) DPPH and superoxide radical scavenging assays of 72.1 ± 0.04% and 38.3 ± 0.16% at 1.6 mg/ml, respectively. The genome consists of a 7,688,855 bp linear chromosome, 6782 protein-coding sequences, and 68 tRNAs. Genomic analysis identified strain VCCM 22513 as Streptomyces parvulus and confirmed a highly conserved core genome and stability of S. parvulus under natural selection. Genome mining revealed the presence of genetic determinants involved in mycothiol and ergothioneine biosynthesis (26 genes), oxidative stress resistance (43 genes), osmoadaptation (87 genes), heat and cold stress (34 genes), aromatic compound degradation (55 genes). Further genome-wide comparison between S. parvulus VCCM 22513 and 11 Streptomyces genomes showed that VCCM 22513 possesses significantly higher copies of genes involved in mycothiol and ergothioneine biosynthesis. In support of this finding, the strain exhibited much resistance to 0.6–1.0 M H2O2 and 6% (w/v) NaCl as compared to Streptomyces cavourensis YBQ59 isolated from Cinnamomum cassia Prels. In addition, the complete pathways for degradation of aromatic compounds including protocatechuate, gentisate, 4-hydroxyphenylpyruvate, cinnamate, 3-phenylpropionate, and styrene were only identified in the genome of VCCM 22513. Conclusions The present study revealed for the first time adaptive responses of mangrove endophytic S. parvulus VCCM 22513 to survive in hostile environment. The information shown here provided better understanding of underlying mechanisms related to adaptation and partially plant-microbe interaction of Streptomyces associated with mangrove plants.