Copper and light shape coastal picophytoplankton communities via their combined effects on growth limitation and toxicity

Copper (Cu) and light are two resources that can limit phytoplankton
growth at very low (deficiency) or very high (toxicity) levels. In this
study, Cu and light interactive effects on picophytoplankton growth and
community composition southern California were assessed during four bottle
incubation experiments using a 7x7 matrix of overlapping Cu and light
gradients. Consistent with prior knowledge, sensitivity to Cu in the two
September experiments was greatest in Prochlorococcus, followed by
Synechococcus, and then picoeukaryotes. Prochlorococcus abundance declined
gradually with Cu additions >6 nM, whereas Synechococcus showed a
sharp toxicity threshold at >10 nM added Cu. Synergistic effects
between Cu and light exacerbated toxicity in both taxa, suggesting that
shared stress response pathways become saturated and less effective when
Cu and light are both high. An unexpected increase in ambient seawater Cu
concentration prior to the two October experiments brought Prochlorococcus
and Synechococcus close to their toxicity thresholds, potentiating their
apparent sensitivity to light and leading to steeper population declines
in the experiments. Addition of 10 mM nitrate at the start of one of the
experiments did not rescue the populations from toxicity, suggesting that
relief of N limitation did not allow for greater acclimation via de novo
stress response enzyme synthesis. Across all experiments, picoeukaryotes
were more resilient to high light and Cu, allowing them to persist or
increase under conditions that limited Prochlorococcus and Synechococcus.
This robustness combined with relief from competition for other resources
(possibly phosphate) upon decline of the other two taxa, ultimately led
picoeukaryotes to dominate the communities despite having very low
baseline relative abundances. Selection for different Synechococcus clades
and picoeukaryote species likely permitted each of these populations to
thrive over a broader range of Cu and light combinations than would be
possible for less biodiverse populations.