Proteorhodopsins dominate the expression of phototrophic mechanisms in seasonal and dynamic marine picoplankton communities

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.

Transcriptional Patterns of Biogeochemically Relevant Marker Genes by Temperate Marine Bacteria

“…We also found a significant correlation between PR transcripts and the abundance of SAR11 in situ (determined by 16S rRNA amplicon sequencing in Alonso-Sáez et al, 2015, Spearman Rho = 0.83, p = 0.015, n = 8). Similarly, in coastal waters of the San Pedro Channel, PR gene transcripts were generally dominated by SAR11 except for a sample collected during a spring algal bloom, where Gammaproteobacteria dominated PR transcripts (Sieradzki et al, 2018). Thus, our results support the idea that community turnover strongly impacts some gene transcriptional patterns (Salazar et al, 2019).…”

Diel changes and diversity of pufM expression in freshwater communities of anoxygenic phototrophic bacteria

“…This may explain the previously mentioned (see Introduction) contradictory reports from marine metatranscriptome studies. While the San Pedro Channel was sampled during the day and resulted in very low expression activity of the APB genes 32 , the samples at the station ALOHA (Hawaii) were collected before sunrise, and the puf genes were among the most actively expressed 31 . Yet, our findings contradict the results of a diel study from an oligotrophic mountain lake Llebreta, reporting expression of BChl-related genes during the day 33 .…”

“…In contrast, Sieradzki et al . 32 have reported very low expression of genes related to anoxygenic phototrophy in their seasonal survey of gene expression in the San Pedro Channel. Even less information is available from freshwater environments.…”

Influence of Light on Particulate Organic Matter Utilization by Attached and Free-Living Marine Bacteria

“…A number of studies have now shown that free-living strict chemoheterotrophy is not the most successful metabolism in surface waters, as the majority of bacteria in these environments are known free-living photoheterotrophs containing genes for proteorhodopsin phototrophy (80–100% of picoplankton genomes) or aerobic anoxygenic photosynthesis (5–30% of genomes; Brindefalk et al, 2016; Dubinsky et al, 2017; Sieradzki et al, 2018). In this study, we identified several free-living OTUs that became numerically enriched in the light compared to the dark, and one that exhibited increased relative isotope incorporation in the light versus the dark.…”