Abstract
Whole transcriptome shotgun sequencing (RNA-seq) was used to assess the transcriptomic response of the toxic cyanobacterium Microcystis aeruginosa during growth with low levels of dissolved inorganic nitrogen (low N), low levels of dissolved inorganic phosphorus (low P), and in the presence of high levels of high molecular weight dissolved organic matter (HMWDOM). Under low N, one third of the genome was differentially expressed, with significant increases in transcripts observed among genes within the nir operon, urea transport genes (urtBCDE), and amino acid transporters while significant decreases in transcripts were observed in genes related to photosynthesis. There was also a significant decrease in the transcription of the microcystin synthetase gene set under low N and a significant decrease in microcystin content per Microcystis cell demonstrating that N supply influences cellular toxicity. Under low P, 27% of the genome was differentially expressed. The Pho regulon was induced leading to large increases in transcript levels of the alkaline phosphatase phoX, the Pst transport system (pstABC), and the sphX gene, and transcripts of multiple sulfate transporter were also significantly more abundant. While the transcriptional response to growth on HMWDOM was smaller (5–22% of genes differentially expressed), transcripts of multiple genes specifically associated with the transport and degradation of organic compounds were significantly more abundant within HMWDOM treatments and thus may be recruited by Microcystis to utilize these substrates. Collectively, these findings provide a comprehensive understanding of the nutritional physiology of this toxic, bloom-forming cyanobacterium and the role of N in controlling microcystin synthesis.
Highlights
One of the most common bloom-forming cyanobacteria in temperate freshwater ecosystems is Microcystis which produces the hepatotoxin microcystin [1,2]
Experimental treatments included a control in which triplicate cultures were grown with replete amounts of N and P (1.0761021 M nitrate, 1.2661023 M orthophosphate (Pi)) and five treatments including low N (75 mM nitrate), low P (0 mM Pi), high molecular weight dissolved organic matter (HMWDOM) (100 mM dissolved organic nitrogen (DON), 0.8 mM Dissolved organic phosphorus (DOP); see below for isolation method) as the sole N and P source, a treatment with HMWDOM supplemented with 1.2661023 M Pi (HMWDOM+P), and a treatment with HMWDOM supplemented with 8.061025 M ammonium (HMWDOM+N)
Differential growth among treatments The control cultures and cultures grown on various treatments of HMWDOM displayed similar growth rates at the time of harvest (0.4460.06) whereas those grown on low N and low P were significantly lower (0.0860.03 and 0.1360.04, respectively; p,0.05, Tukey Test; Table 1, Figure S1)
Summary
One of the most common bloom-forming cyanobacteria in temperate freshwater ecosystems is Microcystis which produces the hepatotoxin microcystin [1,2]. Since many freshwater ecosystems are P-limited [8,9,10,11], P loading is hypothesized to play a key role in the occurrence of many cyanobacteria blooms. Nitrogen loading may influence the occurrence and toxicity of non-diazotrophic toxic cyanobacteria such as Microcystis [15,16]. Recent field studies have demonstrated that N loading can promote blooms of Microcystis [18,19] and laboratory experiments have shown an increase in cellular microcystin content with increasing N levels in Microcystis cultures [20]
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