Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability

Abstract

In vast expanses of the oceans, growth of large phytoplankton such as diatoms is limited by iron availability. Diatoms respond almost immediately to the delivery of iron and rapidly compose the majority of phytoplankton biomass. The molecular bases underlying the subsistence of diatoms in iron-poor waters and the plankton community dynamics that follow iron resupply remain largely unknown. Here we use comparative metatranscriptomics to identify changes in gene expression associated with iron-stimulated growth of diatoms and other eukaryotic plankton. A microcosm iron-enrichment experiment using mixed-layer waters from the northeastern Pacific Ocean resulted in increased proportions of diatom transcripts and reduced proportions of transcripts from most other taxa within 98 h after iron addition. Hundreds of diatom genes were differentially expressed in the iron-enriched community compared with the iron-limited community; transcripts of diatom genes required for synthesis of photosynthesis and chlorophyll components, nitrate assimilation and the urea cycle, and synthesis of carbohydrate storage compounds were significantly overrepresented. Transcripts of genes encoding rhodopsins in eukaryotic phytoplankton were significantly underrepresented following iron enrichment, suggesting rhodopsins help cells cope with low-iron conditions. Oceanic diatoms appear to display a distinctive transcriptional response to iron enrichment that allows chemical reduction of available nitrogen and carbon sources along with a continued dependence on iron-free photosynthetic proteins rather than substituting for iron-containing functional equivalents present within their gene repertoire. This ability of diatoms to divert their newly acquired iron toward nitrate assimilation may underlie why diatoms consistently dominate iron enrichments in high-nitrate, low-chlorophyll regions.RNA-seq | bloom | geoengineering | climate mitigation

Marine diatom proteorhodopsins and their potential role in coping with low iron availability

“…When compared with prokaryotes, all eukaryotic PR genes group together, thus making them appear to be monophyletic (Figure 2b and Figure 5 in Marchetti et al, 2012). Their similarity to PRs within bacteria along with the dispersed presence amongst protist species suggests an initial acquisition from bacteria through horizontal gene transfer followed by subsequent gene losses.…”

“…The P. granii rhodopsin gene (RHO) encodes for the expected seven transmembrane α-helices along with a retinalbinding pocket and a diagnostic residue required for proton transport, making it highly likely that the RHO is proton-pumping rather than sensory (Marchetti et al, 2012). We investigated whether iron and light limitation influenced the expression patterns of P. granii RHO and the subsequent protein abundance.…”

“…The response of eukaryotic phytoplankton to iron enrichment in iron-limited waters of the NE Pacific Ocean was recently investigated using comparative metatranscriptome analyses (Marchetti et al, 2012).…”

Metatranscriptomes reveal functional variation in diatom communities from the Antarctic Peninsula

“…Owing to the global importance of diatoms, genome sequencing projects (Armbrust et al, 2004;Bowler et al, 2008), genome-wide expression analyses Thamatrakoln et al, 2012) and, most recently, environmental metatranscriptomics (Marchetti et al, 2012;Toseland et al, 2013), have provided the most extensive genomic baseline for any phytoplankton group. However, to date, no environmental genomic comparison between Southern Ocean communities has been reported.…”

Considerations for the development and application of control materials to improve metagenomic microbial community profiling

“…RNA may also be a useful proxy for microbial viability. Furthermore, the types of RNA measured may provide an idea of the metabolic challenges facing an environment and assist in explaining why specific microbes predominate in certain environments [14].…”