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Link to original content: https://pubmed.ncbi.nlm.nih.gov/21472017/
Light-induced transcriptional responses associated with proteorhodopsin-enhanced growth in a marine flavobacterium - PubMed Skip to main page content
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. 2011 Oct;5(10):1641-51.
doi: 10.1038/ismej.2011.36. Epub 2011 Apr 7.

Light-induced transcriptional responses associated with proteorhodopsin-enhanced growth in a marine flavobacterium

Hiroyuki Kimura  1 , Curtis R Young, Asuncion Martinez, Edward F Delong
Affiliations

Light-induced transcriptional responses associated with proteorhodopsin-enhanced growth in a marine flavobacterium

Hiroyuki Kimura et al. ISME J. 2011 Oct.

Abstract

Proteorhodopsin (PR) is a photoprotein that functions as a light-driven proton pump in diverse marine Bacteria and Archaea. Recent studies have suggested that PR may enhance both growth rate and yield in some flavobacteria when grown under nutrient-limiting conditions in the light. The direct involvement of PR, and the metabolic details enabling light-stimulated growth, however, remain uncertain. Here, we surveyed transcriptional and growth responses of a PR-containing marine flavobacterium during carbon-limited growth in the light and the dark. As previously reported (Gómez-Consarnau et al., 2007), Dokdonia strain MED134 exhibited light-enhanced growth rates and cell yields under low carbon growth conditions. Inhibition of retinal biosynthesis abolished the light-stimulated growth response, supporting a direct role for retinal-bound PR in light-enhanced growth. Among protein-coding transcripts, both PR and retinal biosynthetic enzymes showed significant upregulation in the light. Other light-associated proteins, including bacterial cryptochrome and DNA photolyase, were also expressed at significantly higher levels in the light. Membrane transporters for Na(+)/phosphate and Na(+)/alanine symporters, and the Na(+)-translocating NADH-quinone oxidoreductase (NQR) linked electron transport chain, were also significantly upregulated in the light. Culture experiments using a specific inhibitor of Na(+)-translocating NQR indicated that sodium pumping via NQR is a critical metabolic process in the light-stimulated growth of MED134. In total, the results suggested the importance of both the PR-enabled, light-driven proton gradient, as well as the generation of a Na(+) ion gradient, as essential components for light-enhanced growth in these flavobacteria.

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Figures

Figure 1
Figure 1
Growth of MED134 incubated in the light or in the dark. MED134 was grown in unenriched ASW (0.05 m C) (a), in ASW enriched to 0.14 m C (b) and in ASW enriched to 0.39 m C (c). The cultures were incubated under continuous white light (○), or in the darkness (•). Error bars denote s.d. for triplicate cultures.
Figure 2
Figure 2
Inventory of RNAs from cultures in the microbial transcriptomic datasets. MED 134 was first incubated in ASW enriched to 0.14 m C in the dark for first 2 days (D2). Then culture was split in two flasks, with one incubated in the light (L2), and the other in the dark (D4), for 2 more days. Numbers in the pie charts represent the percentage of total cDNA reads in each transcriptomic dataset. aSubtraction of 16S and 23S rRNAs were performed after total RNA extraction.
Figure 3
Figure 3
Transcriptomic analyses of proteorhodopsin and retinal biosynthetic genes. (a) Retinal biosynthetic pathway. The colors indicate the L2/D4 ratio of retinal biosynthetic enzymes. The ratio was calculated based on abundance of reads for each specific gene, normalized by the total number of protein-encoding reads for each sample. (b) Cluster analysis of the relative abundance of PR and retinal biosynthetic enzymes. Hierarchical clustering was performed based on the number of cDNA reads, normalized to the total number of protein-encoding cDNAs in each sample, using a Pearson correlation. The heat map shows relative difference of transcript abundance in each sample (red indicates high Pearson correlation; white indicates intermediate; blue indicates low). The numbers of cDNA reads are presented in Table 1. IPP, isopentenyl pyrophosphate; DMAPP, dimethylallyl pyrophosphate; FPP, farnesyl pyrophosphate; GGPP, geranylgeranyl pyrophosphate.
Figure 4
Figure 4
Colony image and growth of MED134 in culture experiments with a specific inhibitor of lycopene cyclization, MPTA. (a, b) Colony pigmentation of MED134 on Marine Agar 2216 (Difco) plate amended with MPTA (a) and without MPTA (b). (c, d) Microbial cell density in enriched ASW (0.14 m C) amended with MPTA in culture exposed to light (▵) and in the dark (▴), and in the enriched ASW without MPTA in culture exposed to light (○) and in the dark (•). Bacterial cells were counted by epifluorescence microscopy (c) and plate count method (d).
Figure 5
Figure 5
Growth of MED134 in cultures incubated with HQNO, a specific inhibitor of Na+-translocating NQR. MED134 was grown in ASW enriched with -alanine (0.7 m C). Cultures were incubated in the ASW amended with HQNO in light (▵) or dark (▴) and in the ASW without HQNO in light (○) or dark (•). Bacterial cell densities were determined by epifluorescence microscopy (a) and plate count method (b).
Figure 6
Figure 6
Model of light-stimulated transcriptional responses in MED134. Proton-pumping processes and retinal biosynthetic pathway are shown in left, whereas central metabolic pathways, such as glycolysis, pentose phosphate cycle, and TCA cycle, are in right. The color of arrows and membrane proteins indicate the value of L2/D4 ratio. The ratio is calculated based on abundance of reads for each gene normalized by total number of protein-encoding reads for each sample. PR, proteorhodopsin; PP, pyrophosphatase; SDH, succinate dehydrogenase; Cyt, cytochrome oxidase; NHA, Na+/H+ antiporter.
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