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

Abstract

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.

The ecological relevance of flagellar motility in soil bacterial communities

“…Consistent with our findings, a recent global classification of life history strategies in bacteria found flagellar motility to be associated with elevated genomic capacity for carbohydrate metabolism, higher 16S rRNA gene copy numbers, and larger genomes [29]. Recent studies focusing on soil bacterial communities have had similar findings [38,46], and in aquatic environments flagellar motility is considered a signature of copiotrophic lifestyles [30]. Overall, our findings suggest that flagellar motility is often part of a general life history strategy for rapid organic carbon metabolism and high maximum potential growth [31], recognizing that these analyses are based on a biased subset of bacterial diversity [44] given that most of the genomes included in this analysis (83%) were derived from cultivated isolates.…”

“…If we could infer the capacity for flagellar motility across a broad diversity of microbial taxa, we could determine the set of traits that generally characterize flagellated taxa (so-called life history strategies; [28, 29]). Previous studies have linked flagellar motility to a fast growth (copiotroph) strategy [30], and flagellar motility is expected to be associated with a life history strategy for rapid nutrient acquisition [31]. However, one of the main challenges with identifying the life history strategies of bacteria remains the quantification of phenotypic traits.…”

Ecological relevance of flagellar motility in soil bacterial communities

“…Consistent with our findings, a recent global classification of life history strategies in bacteria found flagellar motility to be associated with elevated genomic capacity for carbohydrate metabolism, higher 16S rRNA gene copy numbers, and larger genomes [ 29 ]. Recent studies focusing on soil bacterial communities have had similar findings [ 39 , 77 ], and in aquatic environments, flagellar motility is considered a signature of copiotrophic lifestyles [ 30 ]. Overall, our findings suggest that flagellar motility is often part of a general life history strategy for rapid organic carbon metabolism and high maximum potential growth [ 31 ], recognizing that these analyses are based on a biased subset of bacterial diversity [ 76 ] given that most of the genomes included in this analysis (83%) were derived from cultivated isolates.…”

“…If we could infer the capacity for flagellar motility across a broad diversity of microbial taxa, we could determine the set of traits that generally characterize flagellated taxa (so-called life history strategies; [ 28 , 29 ]). Previous studies have linked flagellar motility to a fast growth (copiotroph) strategy [ 30 ], which may be an adaptation to access resource patches [ 31 ], and flagellar motility is expected to be associated with a life history strategy for rapid nutrient acquisition [ 32 ]. However, one of the main challenges with identifying the life history strategies of bacteria remains the quantification of phenotypic traits.…”

Thermophilic Dehalococcoidia with unusual traits shed light on an unexpected past

“…As both flagellar motility and peptidoglycan biosynthesis are energy-intensive, their loss during genome reductions, as evidenced by overall smaller genomes within these orders (Table S2), presumably lowered genetic load and increased fitness of the progenitor of this lineage in niches where flagellar motility and peptidoglycan were not selected for, namely the marine pelagos. 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 [69][70][71]. Many modern pelagic Dehalococcoidia fit this paradigm because MAGs have often been recovered from small cell size fractions (<0.45 µm).…”