Ecotypic variation in phosphorus-acquisition mechanisms within marine picocyanobacteria

Abstract

Prochlorococcus and Synechococcus are major prokaryotic primary producers in the oligotrophic oceans that may be affected by the climate-related increases in nitrogen fixation and subsequent phosphorus (P) limitation in some parts of the oceans. Evidence that Prochlorococcus populations in the North Pacific subtropical gyre (NPSG) have increased over the past decades, possibly due to having a competitive advantage under conditions of P limitation, suggests aspects of their P physiology that are important for dictating their in situ success. Here, we compared the physiology of P acquisition and response to P stress (indicated by alkaline phosphatase activity, APA) among isolates of Prochlorococcus and Synechococcus representing different genotypic clades within the marine picophytoplankton lineage (sensu Urbach et al. 1998: J Mol Evol 46:188-201). The 2 Synechococcus isolates examined (WH 8102 and WH 7803) can utilize a wide variety of organic P sources. Of the 3 Prochlorococcus isolates examined, only the HLI genotype, MED4, is capable of growth on a variety of organic P sources. Under conditions of P starvation the 2 Synechococcus strains and Prochlorococcus MED4 exhibit significant increases in APA, above their measurable constitutive activities. The genomes of the Synechococcus strains and Prochlorococcus MED4 indicate the presence of many P-uptake and -regulatory genes required under conditions of P stress, including the phoA gene that encodes for an alkaline phosphatase enzyme. The other isolates of Prochlorococcus, HLII MIT 9312 and LLIV MIT 9313, have distinctly different P-stress responses. MIT 9312, which contains the same P-uptake and -regulatory genes as MED4, except for psip1 and ptrA, has no constitutive APA, but does exhibit measurable, albeit very low, activity when P starved. MIT 9313, which lacks phoA and a functional phosphate-sensing histidine kinase gene, phoR, exhibits low constitutive activity that decreases when the cells become P-starved. These results show variability in P utilization and in P-stress response between the 2 genera of marine unicellular cyanobacteria, and marked differences among Prochlorococcus genotypes, implying that only certain eco/genotypes of these marine cyanobacteria will have an ecological advantage under conditions of P limitation in the oceans. This further points to the critical need to continue developing genotypic-or cell-specific tools to assess the response of the picophytoplankton community to large-scale changes in nutrient conditions in the oceans.

Potential for phosphite and phosphonate utilization by Prochlorococcus

“…As already observed by Martiny et al (2009), the same Prochlorococcus ecotypes also show an increase in the number of pstS genes in their genomes. Interestingly, this trend is also observed among marine Synechococcus strains (Moore et al, 2005). Moreover, not only does the gene organization of the two phn operons in Prochlorococcus differ (phnDCE and phnCDE), the proteins themselves are also distinct (possessing 27% aa identity) and cluster separately based on protein phylogeny (Figure 2).…”

PtrA is required for coordinate regulation of gene expression during phosphate stress in a marine Synechococcus

“…Comparative genomics (Palenik et al, , 2006Dufresne et al, 2008;Scanlan et al, 2009) and metagenomic surveys (Venter et al, 2004) highlight that there are multiple genomeencoded copies of the gene for the high-affinity, periplasmic P-binding protein, PstS, indicating the importance of the affinity capture of inorganic P, even for strains that have undergone significant genome streamlining (Dufresne et al, 2003). It is also evident that distinct isolates, or ecotypes, show different physiological and genetic capabilities to use organic P (Moore et al, 2005;Martiny et al, 2006;Scanlan et al, 2009). Picocyanobacteria that inhabit low P environments show an overall low requirement for P (Bertilsson et al, 2003;Heldal et al, 2003).…”

Temporal dynamics of Prochlorococcus ecotypes in the Atlantic and Pacific oceans

“…Prochlorococcus is typically the most abundant photoautotroph in tropical and subtropical waters (Campbell et al, 1994;Partensky et al, 1999), and its abundance varies seasonally at some locations (Campbell et al, 1997;DuRand et al, 2001). Studies of cultured isolates have revealed the optimal light and temperature levels differ among the strains (Moore et al, 1998(Moore et al, , 2002Moore and Chisholm, 1999;Zinser et al, 2007), as do the nutrient pools available to them (Moore et al, 2002(Moore et al, , 2005.…”