Characterization of Cyanate Metabolism in Marine Synechococcus and Prochlorococcus spp

Abstract

Cyanobacteria of the genera Synechococcus and Prochlorococcus are the most abundant photosynthetic organisms on earth, occupying a key position at the base of marine food webs. The cynS gene that encodes cyanase was identified among bacterial, fungal, and plant sequences in public databases, and the gene was particularly prevalent among cyanobacteria, including numerous Prochlorococcus and Synechococcus strains. Phylogenetic analysis of cynS sequences retrieved from the Global Ocean Survey database identified >60% as belonging to unicellular marine cyanobacteria, suggesting an important role for cyanase in their nitrogen metabolism. We demonstrate here that marine cyanobacteria have a functionally active cyanase, the transcriptional regulation of which varies among strains and reflects the genomic context of cynS. In Prochlorococcus sp. strain MED4, cynS was presumably transcribed as part of the cynABDS operon, implying cyanase involvement in cyanate utilization. In Synechococcus sp. strain WH8102, expression was not related to nitrogen stress responses and here cyanase presumably serves in the detoxification of cyanate resulting from intracellular urea and/or carbamoyl phosphate decomposition. Lastly, we report on a cyanase activity encoded by cynH, a novel gene found in marine cyanobacteria only. The presence of dual cyanase genes in the genomes of seven marine Synechococcus strains and their respective roles in nitrogen metabolism remain to be clarified.

Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity

“…CynS (PMM0373) encodes a cyanase that converts cyanate to carbon dioxide and ammonia and appears to have a role in cyanate utilization rather than in detoxification in MED4 (Kamennaya and Post, 2011). Intriguingly, under nitrogen-limiting conditions, an asRNA of B300 nt is induced that may have an important role in the regulation of cynS (Figure 4a).…”

A microarray for assessing transcription from pelagic marine microbial taxa

“…Target genes for oligonucleotide probe design were selected based on existing knowledge of gene markers that target microorganism interactions with their environment (for example, Lindell and Post, 2001;Webb et al, 2001;Holtzendorff et al, 2002;Chen et al, 2004;Fuller et al, 2005;Dyhrman and Haley, 2006;Zehr et al, 2007;Orchard et al, 2009;Sebastian and Ammerman, 2009;Kamennaya and Post, 2011;Mosier and Francis, 2011;Paerl et al, 2011). Several genes for hypothetical proteins that were differentially expressed in response to specific stimuli in cultured marine microorganisms were also included (Scanlan et al, 1996;Martiny et al, 2009;Shi et al, 2009;Tetu et al, 2009; et al, 2011).…”

“…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).…”

Distribution and expression of the cyanate acquisition potential among cyanobacterial populations in oligotrophic marine waters

“…Marine Prochlorococcus were reported to consume amino acids (Zubkov et al 2003;Mary et al 2008), and urea is readily assimilated by several Synechococcus and Prochlorococcus isolates (Moore et al 2002;Kamennaya et al 2008;Kamennaya and Post 2010). The latter compound in seawater also spontaneously decomposes to cyanate (Kamennaya et al 2008). A number of Synechococcus and Prochlorococcus strains grow on cyanate as the sole N source (Miller and Espie 1994;Kamennaya et al 2008;Kamennaya and Post 2010).…”

“…Comprehensive studies of N fluxes (Dugdale and Goering 1967;Hansell and Goering 1990) are less common, with the majority of the studies typically neglecting to include dissolved organic N species (e.g., urea and amino acids), though these labile nitrogen compounds are ubiquitous in seawater (Remsen 1971) and are readily utilized by diverse marine phytoplankton species (Dugdale and Goering 1967;Mccarthy 1972;Vargo 1979). Marine Prochlorococcus were reported to consume amino acids (Zubkov et al 2003;Mary et al 2008), and urea is readily assimilated by several Synechococcus and Prochlorococcus isolates (Moore et al 2002;Kamennaya et al 2008;Kamennaya and Post 2010). The latter compound in seawater also spontaneously decomposes to cyanate (Kamennaya et al 2008).…”