Copper toxicity response influences mesotrophic Synechococcus community structure

Abstract

Picocyanobacteria from the genus Synechococcus are ubiquitous in ocean waters. Their phylogenetic and genomic diversity suggests ecological niche differentiation, but the selective forces influencing this are not well defined. Marine picocyanobacteria are sensitive to Cu toxicity, so adaptations to this stress could represent a selective force within, and between, 'species', also known as clades. Here, we compared Cu stress responses in cultures and natural populations of marine Synechococcus from two co-occurring major mesotrophic clades (I and IV). Using custom microarrays and proteomics to characterize expression responses to Cu in the lab and field, we found evidence for a general stress regulon in marine Synechococcus. However, the two clades also exhibited distinct responses to copper. The Clade I representative induced expression of genomic island genes in cultures and Southern California Bight populations, while the Clade IV representative downregulated Fe-limitation proteins. Copper incubation experiments suggest that Clade IV populations may harbour stress-tolerant subgroups, and thus fitness tradeoffs may govern Cu-tolerant strain distributions. This work demonstrates that Synechococcus has distinct adaptive strategies to deal with Cu toxicity at both the clade and subclade level, implying that metal toxicity and stress response adaptations represent an important selective force for influencing diversity within marine Synechococcus populations.

Global proteome response ofSynechocystis6803 to extreme copper environments applied to control the activity of the induciblepetJpromoter

“…The similar increase in copper tolerance during the slow acclimation process has been shown for Synechococcus species (Stuart et al . , ). Thus, by acclimation, we avoided the detrimental, toxic effect of copper ions that has been observed after the shock treatment (Giner‐Lamia et al .…”

“…For example, the toxic effect of copper ions has been observed when >3 lmol l À1 Cu 2+ was added to the copper-free growth medium (Giner-Lamia et al 2012; thereafter, we denote the sharp and drastic increase of copper concentration in the growth medium as the shock treatment. In contrast, slow acclimation to increasing copper concentrations allows cells to successfully survive in otherwise toxic conditions (Shavyrina et al 2001;Stuart et al 2009Stuart et al , 2017.…”

Differential heavy metal sensitivity in seven algal species from the NIES culture collection based on delayed fluorescence assays

“…It is possible that there are stress‐tolerant subgroups within Synechococcus (Stuart et al . ). Since Zn is indispensable in living organisms, its sequestration in vacuoles has been observed in plants exposed to high concentrations (Kobae et al .…”

The Toxicity of Copper to Crocosphaera watsonii and Other Marine Phytoplankton: A Systematic Review

“…We believe that similar disagreement would arise for any species tested using such largely different procedures, as discussed below. Cu-induced growth inhibition has also been studied in both coastal and open ocean cyanobacterial communities in situ (Gustavson and Wängberg, 1995;Moffett et al, 1997;Mann et al, 2002;Broise and Palenik, 2007;Debelius et al, 2009Debelius et al, , 2010Debelius et al, , 2011Paytan et al, 2009;Stuart et al, 2013Stuart et al, , 2017. Although the exact origin and structure of metal-binding ligands remains uncertain, there is evidence that cyanobacteria are major sources of class 1 ligands (Moffett et al, 1990;Moffett and Brand, 1996;Croot et al, 2000;Wiramanaden et al, 2008) and may drive the seasonality of Cu speciation in coastal environments (Croot, 2003).…”

“…Although the exact origin and structure of metal-binding ligands remains uncertain, there is evidence that cyanobacteria are major sources of class 1 ligands (Moffett et al, 1990;Moffett and Brand, 1996;Croot et al, 2000;Wiramanaden et al, 2008) and may drive the seasonality of Cu speciation in coastal environments (Croot, 2003). Conversely, Cu additions can alter cyanobacterial community composition through selective toxicity, and it appears that natural inputs indeed produce a realized niche-partitioning (Moffett et al, 1997;Mann et al, 2002;Stuart et al, 2013Stuart et al, , 2017.…”