Genome-Wide Analysis of Light Sensing inProchlorococcus

Abstract

Prochlorococcus MED4 has, with a total of only 1,716 annotated protein-coding genes, the most compact genome of a free-living photoautotroph. Although light quality and quantity play an important role in regulating the growth rate of this organism in its natural habitat, the majority of known light-sensing proteins are absent from its genome. To explore the potential for light sensing in this phototroph, we measured its global gene expression pattern in response to different light qualities and quantities by using high-density Affymetrix microarrays. Though seven different conditions were tested, only blue light elicited a strong response. In addition, hierarchical clustering revealed that the responses to high white light and blue light were very similar and different from that of the lower-intensity white light, suggesting that the actual sensing of high light is mediated via a blue-light receptor. Bacterial cryptochromes seem to be good candidates for the blue-light sensors. The existence of a signaling pathway for the redox state of the photosynthetic electron transport chain was suggested by the presence of genes that responded similarly to red and blue light as well as genes that responded to the addition of DCMU [3-(3,4-dichlorophenyl)-1,1-N-N-dimethylurea], a specific inhibitor of photosystem II-mediated electron transport.The acclimation of plants and phototrophic microorganisms to the ambient light climate is crucial for survival. All photosynthetic organisms respond to changes in light, including changes in light quantity and quality, i.e., wavelength, by regulating their gene expression. Adaptations to light color detection involve red-light (RL)-, green-light (GL)-, and blue-light (BL)-absorbing receptors, such as phytochromes, cryptochromes, rhodopsins, and xanthopsins (16). Photoreceptors are common to both eukaryotes and prokaryotes, playing important roles in processes such as phototaxis, circadian regulation, and the regulation of flavonoid and alkaloid synthesis (13,17,50).Prochlorococcus is a marine oxyphotobacterium that thrives in the vast oligotrophic gyres of the open ocean between 40°N and 40°S. In these areas, it numerically dominates the phytoplankton, accounting for up to 50% of the total chlorophyll (40, 51). Light appears to have been one of the most important environmental factors driving the speciation and adaptation of Prochlorococcus (36). In the natural environment, Prochlorococcus cells occur from the water surface down to about 200 m (39), experiencing differences in light intensity of over 4 orders of magnitude and a strong spectral shift from white light (WL) to blue light with increasing depth. The ability to grow over this broad range of light intensities is attributed, in part, to the existence of distinct "ecotypes" that have different light optima for growth and different relative abundances with depth in the ocean (1, 9, 24, 53, 56) and constitute distinct phylogenetic clades (24,35,38,44,52).Little is known about photoreceptor-mediated light regulation in Prochloroco...

Genetic diversity in cultured and wild marine cyanomyoviruses reveals phosphorus stress as a strong selective agent

“…Multi-copy hlis have orthologs, such as hli03, in phage (Lindell et al, 2004). Genes in this category are often found in hyper-variable regions in host genomes and are upregulated in response to changes in light (Steglich et al, 2006), iron (Thompson et al, 2011a) and nitrogen (Tolonen et al, 2006) in host cells, as well as stress imposed by phage infection (Lindell et al, 2004(Lindell et al, , 2007. In the case of nitrogen, binding sites for the global nitrogen regulator NtcA were found upstream of hlis with differential transcription under changing nitrogen conditions (Tolonen et al, 2006).…”

“…Hli genes are similar in sequence to chlorophyll a/b-binding proteins that are often upregulated under changes in light intensity in cyanobacteria (Dolganov et al, 1995;Funk and Vermaas, 1999;Bhaya et al, 2002;Steglich et al, 2006). There are numerous hlis in Prochlorococcus genomes (Coleman and Chisholm, 2007).…”

Transcriptional response of Prochlorococcus to co-culture with a marine Alteromonas: differences between strains and the involvement of putative infochemicals

“…Instead, many genes encoding HLIPs were more abundantly expressed in this co-culture, whereas these genes were primarily less abundantly expressed in MED4+1A3 and 9313+diluted 1A3, the two co-cultures where Prochlorococcus was not inhibited (Table 2). HLIPs are short peptides previously suggested to be involved in photoacclimation (Steglich et al, 2006;Berg et al, 2011), but which may respond also to various stresses (Tolonen et al, 2006) (Supplementary information). We interpret these results to suggest that the photosystem in the 9313+1A3 co-culture is exposed to significantly more stress than the other two co-cultures, and that this stress is different from that caused by a shift in light intensity or by nutrient stress.…”

Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus

“…PTOX transfers electrons from plastoquinone to molecular oxygen to form water, and is thus involved in photoacclimation and maintaining cellular redox poise during high light conditions. Indeed, decreases in Prochlorococcus PTOX expression have been observed in 3-(3,4-dichlorophenyl)-1,1-N-N'-dimethylurea (DCMU)-treated cells (Steglich et al, 2006); DCMU is an inhibitor of PSII-mediated electron transport that causes a net oxidation of the plastoquinone pool. In addition, Prochlorococcus PTOX expression has been shown to increase during conditions of CO 2 limitation (Bagby and Chisholm, 2015), reinforcing the role of this enzyme as a 'safety valve' for the cell and implicating the decrease in PTOX transcript abundance seen here in co-culture as a reflection of generally reduced stress on the cells.…”