Aquatic bacteria frequently are divided into lifestyle categories oligotroph or copiotroph. Oligotrophs have proportionately fewer transcriptional regulatory genes than copiotrophs and are generally non-motile/chemotactic. We hypothesized that the absence of chemotaxis/motility in oligotrophs prevents them from occupying nutrient patches long enough to benefit from transcriptional regulation. We first confirmed that marine oligotrophs are generally reduced in genes for transcriptional regulation and motility/chemotaxis. Next, using a non-motile oligotroph (Ca. Pelagibacter st. HTCC7211), a motile copiotroph (Alteromonas macleodii st. HOT1A3), and [ 14 C]L-alanine, we confirmed that L-alanine catabolism is not transcriptionally regulated in HTCC7211 but is in HOT1A3. We then found that HOT1A3 took 2.5-4 min to initiate L-alanine oxidation at patch L-alanine concentrations, compared to <30 s for HTCC7211. By modelling cell trajectories, we predicted that, in most scenarios, non-motile cells spend <2 min in patches, compared to >4 min for chemotactic/motile cells. Thus, the time necessary for transcriptional regulation to initiate prevents transcriptional regulation from being beneficial for non-motile oligotrophs. This is supported by a mechanistic model we developed, which predicted that HTCC7211 cells with transcriptional regulation of L-alanine metabolism would produce 12% of their standing ATP stock upon encountering an L-alanine patch, compared to 880% in HTCC7211 cells without transcriptional regulation.
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.
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