Responses to iron limitation are impacted by light quality and regulated by RcaE in the chromatically acclimating cyanobacterium Fremyella diplosiphon

Abstract

Photosynthetic organisms adapt to environmental fluctuations of light and nutrient availability. Iron is critical for photosynthetic organismal growth, as many cellular processes depend upon iron cofactors. Whereas low iron levels can have deleterious effects, excess iron can lead to damage, as iron is a reactive metal that can result in the production of damaging radicals. Therefore, organisms regulate cellular iron levels to maintain optimal iron homeostasis. In particular, iron is an essential factor for the function of photosystems associated with photosynthetic light-harvesting complexes. Photosynthetic organisms, including cyanobacteria, generally respond to iron deficiency by reduced growth, degradation of non-essential proteins and in some cases alterations of cellular morphology. In response to fluctuations in ambient light quality, the cyanobacterium Fremyella diplosiphon undergoes complementary chromatic adaptation (CCA). During CCA, phycobiliprotein composition of light-harvesting antennae is altered in response to green light (GL) and red light (RL) for efficient utilization of light energy for photosynthesis. We observed light-regulated responses to iron limitation in F. diplosiphon. RL-grown cells exhibited significant reductions in growth and pigment levels, and alterations in iron-associated proteins, which impact the accumulation of reactive oxygen species under iron-limiting conditions, whereas GL-grown cells exhibited partial resistance to iron limitation. We investigated the roles of known CCA regulators RcaE, RcaF and RcaC in this light-dependent iron-acclimation response. Through comparative analyses of wild-type and CCA mutant strains, we determined that photoreceptor RcaE has a central role in light-induced oxidative stress associated with iron limitation, and impacts light-regulated iron-acclimation responses, physiologically and morphologically.

Molecular basis and fitness implications of the interplay between light and the regulation of iron homeostasis in photosynthetic organisms

“…It has been proposed that light-dependent regulation of FRO6 occurs in a tissue-specific and/or developmentally regulated way in plants to coordinate iron acquisition with external developmental and environmental cues (Feng et al, 2006). Notably, a similar coordination of iron responses and external environmental cues may occur in other organisms including cyanobacteria (see below; Pattanaik et al, 2014). As FRO6 mRNA levels are regulated by light, it is anticipated that specific photoreceptors contribute to its expression.…”

“…cyanobacteria. Cross talk between light quality/intensity and iron limitation has been observed for Fremyella diplosiphon (Pattanaik et al, 2014;Pattanaik and Montgomery, 2010). Whereas wild-type cells grown under red light in iron-limited medium show classic iron-deficient symptoms such as photosynthetic pigment defects, wild-type cells grown under green light show minor responses to iron limitation (Pattanaik and Montgomery, 2010).…”

“…Whereas wild-type cells grown under red light in iron-limited medium show classic iron-deficient symptoms such as photosynthetic pigment defects, wild-type cells grown under green light show minor responses to iron limitation (Pattanaik and Montgomery, 2010). RcaE, a cyanobacterial photoreceptor that is related to higher plant phytochromes (Kehoe and Grossman, 1996;Terauchi et al, 2004), impacts the observed light-regulated iron homeostasis responses in the cyanobacterium F. diplosiphon as an RcaE-deficient mutant shows resistance to iron limitation under both red and green illumination (Pattanaik et al, 2014). Light and iron also have impacts on cellular morphology (Pattanaik et al, 2014;Pattanaik and Montgomery, 2010).…”

“…RcaE, a cyanobacterial photoreceptor that is related to higher plant phytochromes (Kehoe and Grossman, 1996;Terauchi et al, 2004), impacts the observed light-regulated iron homeostasis responses in the cyanobacterium F. diplosiphon as an RcaE-deficient mutant shows resistance to iron limitation under both red and green illumination (Pattanaik et al, 2014). Light and iron also have impacts on cellular morphology (Pattanaik et al, 2014;Pattanaik and Montgomery, 2010). Red light appears to augment the effect of iron limitation on F. diplosiphon both at the level of growth and the regulation of stress-induced changes in cellular morphology (Pattanaik et al, 2014;Pattanaik and Montgomery, 2010).…”

“…Light and iron also have impacts on cellular morphology (Pattanaik et al, 2014;Pattanaik and Montgomery, 2010). Red light appears to augment the effect of iron limitation on F. diplosiphon both at the level of growth and the regulation of stress-induced changes in cellular morphology (Pattanaik et al, 2014;Pattanaik and Montgomery, 2010). This response is regulated as the light quality-dependent difference in iron limitation-associated morphology changes does not occur in a mutant lacking the primary red and green light-responsive photosensory receptor RcaE (Pattanaik et al, 2014).…”