Differences in the regulatory strategies of marine oligotrophs and copiotrophs reflect differences in motility

Aquatic bacteria are frequently divided into the lifestyle categories oligotroph or copiotroph, reflecting adaptations to low and high nutrient availability. In aquatic ecosystems, copiotrophy is associated with chemotaxis and motility, which cells use to find and occupy high-nutrient patches. Oligotrophs have proportionately fewer transcriptional regulatory proteins than copiotrophs, and some have been shown to constitutively express genes involved in the uptake and oxidation of carbon compounds. We hypothesized that the absence of chemotaxis/motility in oligotrophs might prevent them from occupying nutrient patches long enough to benefit from transcriptional regulation. To test this hypothesis, we measured uptake and oxidation of a radiolabeled amino acid, [14C]L-alanine, by a non-motile oligotroph (Ca. Pelagibacter st. HTCC7211) and a motile copiotroph (Alteromonas macleodii st. HOT1A3). We found that L-alanine catabolism is not transcriptionally regulated in HTCC7211 but is in HOT1A3, initiating within 2.5 – 4 min, as supported by RT-qPCR experiments. L-alanine uptake in HTCC7211 was modulated within 30s by low-amplitude (2-fold) post-translational regulation, a conclusion supported by quantitative analysis with a mechanistic model. By modeling cell trajectories under a range of patch conditions, we predicted that, in most scenarios, non-motile cells spend <2 min in patches, while chemotactic/motile cells occupy patches >4 mins. We conclude that the time necessary to initiate transcriptional regulation prevents non-motile oligotrophs, which drift with currents, from benefiting from transcriptional regulation, but instead have low-amplitude post-translational regulation that can take advantage of their transient passage through a patch. Importance Some aquatic oligotrophic bacteria eschew the usual strategy of transcriptionally regulating genes for carbon uptake and metabolism, instead continuously expressing these systems whether the corresponding carbon compounds are present or not. Often, aquatic oligotrophs lack chemotaxis and motility, while their copiotrophic counterparts use chemotaxis/motility to maximize time spent in patches of high nutrients. We show that diminished transcriptional regulation of carbon catabolism in oligotrophs is due to time limitations: transcriptional regulation takes time, and oligotrophs do not have enough time in nutrient patches for transcriptional regulation to be useful because of their lack of motility. This work enhances our knowledge of the carbon oxidation strategies of marine bacterioplankton and lays the foundation for further theoretical work on this subject.