Abstract
The most abundant and ubiquitous microbes in the surface ocean use light as an energy source, capturing it via complex chlorophyll-based photosystems or simple retinal-based rhodopsins. Studies in various ocean regimes compared the abundance of these mechanisms, but few investigated their expression. Here we present the first full seasonal study of abundance and expression of light-harvesting mechanisms (proteorhodopsin, PR; aerobic anoxygenic photosynthesis, AAnP; and oxygenic photosynthesis, PSI) from deep-sequenced metagenomes and metatranscriptomes of marine picoplankton (<1 µm) at three coastal stations of the San Pedro Channel in the Pacific Ocean. We show that, regardless of season or sampling location, the most common phototrophic mechanism in metagenomes of this dynamic region was PR (present in 65–104% of the genomes as estimated by single-copy recA), followed by PSI (5–104%) and AAnP (5–32%). Furthermore, the normalized expression (RNA to DNA ratio) of PR genes was higher than that of oxygenic photosynthesis (average ± standard deviation 26.2 ± 8.4 vs. 11 ± 9.7), and the expression of the AAnP marker gene was significantly lower than both mechanisms (0.013 ± 0.02). We demonstrate that PR expression was dominated by the SAR11-cluster year-round, followed by other Alphaproteobacteria, unknown-environmental clusters and Gammaproteobacteria. This highly dynamic system further allowed us to identify a trend for PR spectral tuning, in which blue-absorbing PR genes dominate in areas with low chlorophyll-a concentrations (<0.25 µgL−1). This suggests that PR phototrophy is not an accessory function but instead a central mechanism that can regulate photoheterotrophic population dynamics.
Highlights
Sunlight is the most readily available source of energy in the photic zone of the ocean
Light utilization in marine microorganisms is divided between complex, high-yield photosystems and simple, low-yield rhodopsins (Finkel et al, 2013)
We found that the high-resolution expression patterns were much less even than gene distribution, where the top 10 most highly expressed leaves generally accounted for >70% of the SAR11 prd transcripts compared to less than 50% of gene abundance
Summary
Sunlight is the most readily available source of energy in the photic zone of the ocean. Lightdriven proton pump PRs can increase the membrane potential of the cell, supporting a variety of processes such as ATP synthesis (Béjà et al, 2000; Walter et al 2007; Steindler et al.2011), substrate uptake (Steindler et al 2011; Gómez-Pereira et al 2013; Gómez-Consarnau et al 2016), survival during starvation (Gómez-Consarnau et al 2010; Steindler et al 2011) and/or salinity stress response (Feng et al 2013) Taken together, their structural simplicity and the range of functions they can support seem to have promoted the expansion of microbial rhodopsins in the sunlit ocean. In contrast to qPCR methods, generation sequencing techniques can provide more reliable estimates without introducing qPCR and cloning biases that would miss certain PR gene types (Nguyen et al, 2015; Boeuf et a. 2016)
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