Contrasting mechanisms of proteomic nitrogen thrift in Prochlorococcus

Abstract

Organisms limited by carbon, nitrogen or sulphur can reduce protein production costs by transitions to less costly amino acids, or by reducing protein expression. These alternative mechanisms of nutrient thrift might respond differently to selection, but this possibility remains untested. We hypothesized that relatively invariant sequence composition responds to long-term variation in nutrient concentrations, whereas dynamic expression profiles vary with nutrient predictability. Prolonged nutrient scarcity favours proteome-wide nutrient reduction. Under stable, nonfluctuating nutrient availability, reduction of nutrient content typically occurs in proteins upregulated when nutrient availability is low, e.g. assimilation and catabolism. We suggest that fluctuating nutrient availability favours mechanisms involving short-term downregulation of nutrient-rich proteins. We analysed protein nitrogen content in six high-light, low-nutrient adapted (HL) vs. six low-light, high-nutrient adapted (LL) Prochlorococcus (marine cyanobacteria) strains, alongside expression data under experimental nitrogen and phosphorus limitation in two strains, MED4 (HL) vs. MIT9313 (LL). HL strains contained less nitrogen, but DNA GC content confounded this relationship. While anabolic and catabolic proteins had normal nitrogen content, most strains showed reduced nitrogen in typical nitrogen stress response proteins. In the experimental data set, though, proteins upregulated under nitrogen limitation were nitrogen-poor only in MIT9313, not MED4. MIT9313 responded similarly to nitrogen and phosphorus limitation, with slow, sustained downregulation of nitrogen-rich ribosomal proteins. In contrast, under nitrogen but not phosphorus limitation, MED4 rapidly downregulated ribosomal proteins. MED4's specific, rapid nitrogen response suggests adaptation to fluctuating conditions, supporting previous work. Thus, we identify contrasting proteomic nitrogen thrift mechanisms within Prochlorococcus consistent with different nutrient regimes.