Genomic adaptation of marine phytoplankton populations regulates phosphate uptake

Abstract

In this study, we combined “reciprocal transplant experiments,” cell‐sorting, and metagenomics to understand how phytoplankton adapt to differences in phosphate availability and the implications for nutrient uptake rates. Reciprocal transplant experiments were conducted on six stations ranging from cold, nutrient‐rich water in the Labrador Sea to warm, extremely P‐deplete water in the Sargasso Sea. In most cases, the direct impact of environmental conditions and likely P availability was the strongest control on phosphate uptake. However, especially the transplant experiments between the northern and southern stations revealed that there are situations where changes in community composition and functional genes have an important effect on uptake rates. Phytoplankton lineages responded uniquely to changing environmental conditions. The picoeukaryotic phytoplankton P uptake response was strongly regulated by the phosphate concentration, whereas the effect of community composition was larger for Prochlorococcus and Synechococcus. In support, we found a tight negative relationship between ambient phosphate concentration and the frequency of P acquisition genes in both Prochlorococcus and Synechococcus, and such differences in genome content could be linked to lineage‐specific shifts in uptake rates. Linking genes with ocean biogeochemistry is a major scientific and technical challenge and most studies rely on correlations between genotypes and environmental conditions. However, our study demonstrates how reciprocal transplant experiments are a possible tool for understanding the relative role of environmental condition vs. plankton diversity in regulating important open ocean ecosystem processes.

A meta-analysis on environmental drivers of marine phytoplankton C : N : P

“…Another plausible hypothesis concerns variability in the acclimation/adaptation strategy at the genetic level (Dyhrman, 2016). Recent studies suggest that different phytoplankton groups exhibit different levels of transcriptional responsiveness and have different strategies for using nitrate (Lampe et al, 2019) and phosphate (Martiny et al, 2019). For example, diatoms have superior abilities to uptake and store nutrients by being able to quickly regulate their gene expression patterns required for nutrient uptake compared to other phytoplankton groups (Cáceres et al, 2019;Lampe et al, 2018Lampe et al, , 2019.…”

“…(2) increase in nutrient use efficiency which enables greater carbon fixation for given nutrient availability; and (3) translation compensation theory, which predicts that less P-rich ribosomes are required for protein synthesis and growth as the translation process becomes kinetically more efficient (McKew et al, 2015;Toseland et al, 2013;Woods et al, 2003;Xu et al, 2014;Zhu et al, 2017).…”

A meta-analysis on environmental drivers of marine phytoplankton C : N : P

“…phosphate (Martiny et al, 2019b) uses. In particular, diatoms have superior abilities to uptake and store nutrients by being able to quickly regulate their gene expression patterns required for nutrient uptake compared to other phytoplankton groups (Cáceres et al, 2019;Lampe et al, 2018Lampe et al, , 2019.…”

Variable inter and intraspecies alkaline phosphatase activity within single cells of revived dinoflagellates

“…Even though these approaches can demonstrate how phytoplankton respond to changes in temperature, nutrients and heavy metals, they remain limited to short-term incubations (e.g. weeks or months) because phytoplankton experiments are cumbersome to be carried out for longer periods [14][15][16][17]. For studying long-term physiological variations within phytoplankton species, an innovative approach consists of comparing biological functions among strains of species revived from sediments of different ages.…”