Proteorhodopsin light-enhanced growth linked to vitamin-B1 acquisition in marine Flavobacteria

Gómez‐Consarnau, Laura; González, José M.; Riedel, Thomas; Jaenicke, Sebastian; Wagner‐Döbler, Irene; Sañudo‐Wilhelmy, Sergio A.; Fuhrman, Jed A.

doi:10.1038/ismej.2015.196

Cited by 49 publications

(65 citation statements)

References 60 publications

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“…strains MED134 and DSW-1 T on the one hand and strain PRO95 on the other hand are linked to vitamin B 1 acquisition. Thus, the authors suggested that the former two species, which are vitamin B 1 auxotrophs, efficiently use light to take up vitamin B 1 from their surroundings, while the latter species, which is a vitamin B 1 autotroph, is inefficient in vitamin B 1 uptake and thus needs to spend substantial energy on vitamin synthesis (150). These findings provide an important impetus to investigate the ecological settings under which rhodopsin photoheterotrophy provides fitness benefits.…”

Section: Light-stimulated Growth Of Naturally Proteorhodopsincontainimentioning

confidence: 99%

“…In Dokdonia sp. MED134, PR gene expression levels are substantially higher upon growth in the light than with growth in darkness (65,117,135,150) (Fig. 5).…”

Section: Light-stimulated Growth Of Naturally Proteorhodopsincontainimentioning

confidence: 99%

“…Genomewide gene expression analysis of PRO95 cells in half-strength marine broth or artificial seawater showed that rhodopsins as well as associated retinal synthesis genes were expressed under these conditions. Gómez-Consarnau et al (150) recently found compelling indications from gene expression analyses that differences in growth responses to light between the closely related Dokdonia sp. strains MED134 and DSW-1 T on the one hand and strain PRO95 on the other hand are linked to vitamin B 1 acquisition.…”

Section: Light-stimulated Growth Of Naturally Proteorhodopsincontainimentioning

confidence: 99%

See 2 more Smart Citations

Marine Bacterial and Archaeal Ion-Pumping Rhodopsins: Genetic Diversity, Physiology, and Ecology

Pinhassi

DeLong

Béjà

et al. 2016

Microbiol Mol Biol Rev

166

160

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SUMMARYThe recognition of a new family of rhodopsins in marine planktonic bacteria, proton-pumping proteorhodopsin, expanded the known phylogenetic range, environmental distribution, and sequence diversity of retinylidene photoproteins. At the time of this discovery, microbial ion-pumping rhodopsins were known solely in haloarchaea inhabiting extreme hypersaline environments. Shortly thereafter, proteorhodopsins and other light-activated energy-generating rhodopsins were recognized to be widespread among marine bacteria. The ubiquity of marine rhodopsin photosystems now challenges prior understanding of the nature and contributions of “heterotrophic” bacteria to biogeochemical carbon cycling and energy fluxes. Subsequent investigations have focused on the biophysics and biochemistry of these novel microbial rhodopsins, their distribution across the tree of life, evolutionary trajectories, and functional expression in nature. Later discoveries included the identification of proteorhodopsin genes in all three domains of life, the spectral tuning of rhodopsin variants to wavelengths prevailing in the sea, variable light-activated ion-pumping specificities among bacterial rhodopsin variants, and the widespread lateral gene transfer of biosynthetic genes for bacterial rhodopsins and their associated photopigments. Heterologous expression experiments with marine rhodopsin genes (and associated retinal chromophore genes) provided early evidence that light energy harvested by rhodopsins could be harnessed to provide biochemical energy. Importantly, some studies with native marine bacteria show that rhodopsin-containing bacteria use light to enhance growth or promote survival during starvation. We infer from the distribution of rhodopsin genes in diverse genomic contexts that different marine bacteria probably use rhodopsins to support light-dependent fitness strategies somewhere between these two extremes.

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Section: Light-stimulated Growth Of Naturally Proteorhodopsincontainimentioning

confidence: 99%

“…In Dokdonia sp. MED134, PR gene expression levels are substantially higher upon growth in the light than with growth in darkness (65,117,135,150) (Fig. 5).…”

Section: Light-stimulated Growth Of Naturally Proteorhodopsincontainimentioning

confidence: 99%

Section: Light-stimulated Growth Of Naturally Proteorhodopsincontainimentioning

confidence: 99%

See 1 more Smart Citation

Marine Bacterial and Archaeal Ion-Pumping Rhodopsins: Genetic Diversity, Physiology, and Ecology

Pinhassi

DeLong

Béjà

et al. 2016

Microbiol Mol Biol Rev

166

160

View full text Add to dashboard Cite

show abstract

“…We further hypothesize that this process may have been more efficient in the light due to proteorhodopsin photoheterotrophy. Flavobacteria TonB transporters, which rely on proton gradients, have been shown to be highly expressed during the peak of algal blooms (Teeling et al 2012), suggesting a role of PR electrochemical gradients in these transport processes (Gómez-Consarnau et al 2016). It therefore seems plausible that, in the marine environment, the first stages of diatom biomass degradation would generally be carried out mostly by photoheterotrophic Flavobacteria still in the photic zone, and that the subsequent stages of organic matter degradation would take place regardless of light as particles sink below the photic zone.…”

Section: Bacterial Dynamics Of Phytodetrital Particle Degradationmentioning

confidence: 99%

Influence of light on particulate organic matter utilization by attached and free-living marine bacteria

Gómez‐Consarnau

Needham

Weber

et al. 2019

Preprint

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1 While the impact of light on primary productivity in aquatic systems has been studied for decades, the role light plays in the degradation of photosynthetically-produced biomass is less well understood. We investigated the patterns of light-induced particle breakdown and bacterial assimilation of detrital C and N using 13 C and 15 N labeled freeze-thawed diatom cells incubated in laboratory microcosms with a marine microbial community freshly-collected from the Pacific Ocean. Particles incubated in the dark resulted in increased bacterial counts and dissolved organic carbon concentrations compared to those incubated in the light. Light also influenced the attached and free-living microbial community structure as detected by 16S rRNA gene amplicon sequencing. For example, bacterial taxa from the Sphingobacteriia were enriched on dark-incubated particles and taxa from the family Flavobacteriaceae and the genus Pseudoalteromonas were numerically enriched on particles in the light. Isotope incorporation analysis by phylogenetic microarray and NanoSIMS (a method called Chip-SIP) identified free-living and attached microbial taxa able to incorporate N and C from the particles. Some taxa, including members of the Flavobacteriaceae and Cryomorphaceae, exhibited increased isotope incorporation in the light, suggesting the use of photoheterotrophic metabolisms. In contrast, some members of Oceanospirillales and Rhodospirillales showed decreased isotope incorporation in the light, suggesting that their heterotrophic metabolism, particularly when occurring on particles, might increase at night or may be inhibited by sunlight. These results show that light influences particle degradation and C and N incorporation by attached bacteria, suggesting that the transfer between particulate and free-living phases are likely affected by external factors that change with the light regime, such as time of day, depth and season.

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“…Rhodopsins are usually associated with a response to survive periods of low nutrient availability (G omez-Consarnau et al, 2010;Kimura et al, 2011;Steindler et al, 2011). However, recent studies suggest that rhodopsin activity may also be related to diverse environmental factors such as salinity (Feng et al, 2013), vitamin auxotrophy (G omez- Consarnau et al, 2016) or the availability of a particular substrate (Xing et al, 2015). Although the benefits conferred by rhodopsins on microorganisms remain poorly understood, the ability to synthesize these photoactive compounds appears to represent a significant adaptive feature in oligotrophic environments (G omez-Consarnau et al, 2010;Kimura et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Evidence of microbial rhodopsins in Antarctic Dry Valley edaphic systems

Guerrero

Vikram

Makhalanyane

et al. 2017

Environmental Microbiology

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Microorganisms able to synthesize rhodopsins have the capacity to translocate ions through their membranes, using solar energy to generate a proton motive force. Rhodopsins are the most abundant phototrophic proteins in oceanic surface waters and are key constituents in marine bacterial ecology. However, it remains unclear how rhodopsins are used in most microorganisms. Despite their abundance in marine and fresh-water systems, the presence of functional rhodopsin systems in edaphic habitats has never been reported. Here, we show the presence of several new putative H , Na and Cl pumping rhodopsins identified by metagenomic analysis of Antarctic desert hypolithic communities. Reconstruction of two Proteobacteria genomes harboring xanthorhodopsin-like proteins and one Bacteroidetes genome with a Na-pumping-like rhodopsin indicated that these bacteria were aerobic heterotrophs possessing the apparent capacity for the functional expression of rhodopsins. The existence of these protein systems in hypolithic bacteria expands the known role of rhodopsins to include terrestrial environments and suggests a possible predominant function as heterotrophic energy supply proteins, a feasible microbial adaptation to the harsh conditions prevalent in Antarctic edaphic systems.

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Proteorhodopsin light-enhanced growth linked to vitamin-B1 acquisition in marine Flavobacteria

Cited by 49 publications

References 60 publications

Marine Bacterial and Archaeal Ion-Pumping Rhodopsins: Genetic Diversity, Physiology, and Ecology

Marine Bacterial and Archaeal Ion-Pumping Rhodopsins: Genetic Diversity, Physiology, and Ecology

Influence of light on particulate organic matter utilization by attached and free-living marine bacteria

Evidence of microbial rhodopsins in Antarctic Dry Valley edaphic systems

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