Ni Uptake and Limitation in MarineSynechococcusStrains

Abstract

Ni accumulation and utilization were studied in two strains of marine Synechococcus, isolated from both coastal (CC9311; clade I) and open-ocean (WH8102; clade III) environments, for which complete genome sequences are available. Both strains have genes encoding an Ni-containing urease and when grown on urea without Ni become Ni-N colimited. The Ni requirements of these strains also depend upon the genomic complement of genes encoding superoxide dismutase (SOD). WH8102, with a gene encoding only an Ni-SOD, has a novel obligate requirement for Ni, regardless of the N source. Reduced SOD activity in Ni-depleted cultures of WH8102 supports the link of this strain's Ni requirement to Ni-SOD. The genome of CC9311 contains a gene for a Cu/Zn-SOD in addition to a predicted pair of Ni-SODs, yet this strain cannot grow without Ni on NO 3 ؊ and can grow only slowly on NH 4 ؉ without Ni, implying that the Cu/Zn-SOD cannot completely replace Ni-SOD in marine cyanobacteria. CC9311 does have a greater tolerance for Ni starvation. Both strains increase their Ni uptake capabilities and actively bioconcentrate Ni in response to decreasing extracellular and intracellular Ni. The changes in Ni uptake rates were more pronounced in WH8102 than in CC9311 and for growth on urea or nitrate than for growth on ammonia. These results, combined with an analysis of fully sequenced marine cyanobacterial genomes, suggest that the growth of many marine Synechococcus and all Prochlorococcus strains is dependent upon Ni.

A microarray for assessing transcription from pelagic marine microbial taxa

“…If microbial taxa were P limited, P addition would result in decreased transcription of P-stress genes and increased transcription of genes for energy metabolism, DNA replication and cell division. However, we expected to see heterogeneous transcriptional responses from individual taxa owing to differences in their genomic capabilities, nutrient requirements and life strategies (Tolonen et al, 2006;Dupont et al, 2008;Ilikchyan et al, 2009;Stuart et al, 2009;Tetu et al, 2009;Kamennaya and Post, 2011;Thompson et al, 2011).…”

Urea and nickel utilization in marine cyanobacteria as evaluated by incubation, proteomic, and uptake techniques

“…If a similar mechanism was at work in the bottle incubation, the newly fixed nitrogen would not have been accounted for in the initial nitrogen store (T 0 in Table 5 and Figure 7) and by displacing a portion of the apparent nitrogen consumption would yield a lower N:P drawdown ratio. Moreover, NiSOD was observed in the same upwelling waters where this incubation was performed ( Figure 8) and this metalloprotein has been shown to be important in some Synechococcus strains that cannot completely substitute alternative non-nickel SOD enzymes (Dupont et al 2008). …”

“…Genomic evidence shows that the cytoplasmic soluble nickel-containing urease is common in cyanobacteria and with low environmental urea concentrations it is suggested by Collier et al (1999) that a high-affinity urea transport system should exist. However, urease is also noted as a constitutive enzyme and internal cycling of urea can be independent from assimilation of external urea for phytoplankton nutrition (Valladares et al 2002;Dupont et al 2008;Nunn et al 2009;Allen et al 2011), even for a diatom strain of Cyclotella when grown on nitrate in the absence of urea (Oliveira and Antia 1986). Genomic and transcriptomic tools have brought new insight into the importance of urea.…”

“…Urease involvement in the ornithine cycle results in a constitutive use of this enzyme (Nunn et al 2009;Allen et al 2011) making nickel an essential nutrient for many phytoplankton. Dupont et al (2008) demonstrated the importance of nickel to marine Synechococcus owing to both urease and nickel-SOD (NiSOD). NiSOD is associated with nitrogen fixation as it protects nitrogenase from superoxide inhibition as shown in the non-heterocyst diazotroph, Trichodesmium by Ho (2013).…”

The cobalt cycle in the Tropical Pacific Ocean

“…In ironlimited cultures, nickel quotas were substantially higher than under cobalt limitation (Fig. 6), perhaps due an increased need for Ni-superoxide dismutase enzyme to counter reactive oxygen stress generated from iron starvation (Dupont et al, 2008. At low Fe, Mn and Co quotas did not increase to the same degree, making it unlikely that Ni was acquired through the Mn transporter (Fig.…”