Morphophysiological and transcriptome analysis reveals a multiline defense system enabling cyanobacterium Leptolyngbya strain JSC-1 to withstand iron induced oxidative stress

Abstract

Iron intoxications induce severe oxidative stress by producing reactive oxygen species (ROS) in cyanobacteria, leading to membrane lipid peroxidation, altered morphology, impaired photosynthesis and other oxidative stress injuries. Given these stresses, mitigation of ROS is a prerequisite for all aerobic organisms. Study of siderophilic cyanobacterium Leptolyngbya strain JSC-1 inhabiting iron-rich hot springs may provide insight into the mechanism of iron homeostasis and alleviation of oxidative stress. In this study, we investigated the morphophysiological and molecular mechanisms enabling this cyanobacterium to cope with iron-induced oxidative stress. Strain JSC-1 biomineralized extracellular iron via an exopolymeric sheath (acting as a first line of defense) and intracellular iron via polyphosphate inclusions (second line of defense), thus minimizing the burden of free ferric ions. Physiological parameters, SOD, CAT and POD activities, bacterioferritin and total protein contents fluctuated in response to iron elevation, displaying a third line of defense to mitigate ROS. Differential gene expression analysis of JSC-1 indicated up-regulation of 94 and 125 genes and down-regulation of 89 and 183 genes at low (4 μM) and high (400 μM) iron concentration, respectively. The differentially expressed genes (DEGs) were enriched in 100 KEGG pathways and were found to be involved in lipopolysaccharide and fatty acid biosynthesis, starch, sucrose, chlorophyll and other metabolic pathways. Together with metabolic reprogramming (fourth line of defense), JSC-1 established a unique multiline defense system that allows JSC-1 to withstand severe oxidative stress. These findings also provide insight into potential survival strategies of ancient microorganisms inhabiting similar environment present in early earth history.