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

Abstract

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.

Thermophilic Dehalococcoidia with unusual traits shed light on an unexpected past

“…As both flagellar motility and peptidoglycan biosynthesis are energy-intensive, these losses presumably lowered genetic load and increased fitness of the progenitor of this lineage in niches where flagellar motility and peptidoglycan were not selected for, including the marine pelagos and deep-sea sediments. Motility is rare among pelagic oligotrophs with small cell size due to nutrient limitations and the high effect of Brownian motion on small cells, resulting in inefficient swimming at a high energy cost [65][66][67] . Modern pelagic Dehalococcoidia fit this paradigm because many MAGs have been recovered from small cell size fractions (< 0.45 µm).…”