Conditional filamentation as an adaptive trait of bacteria and its ecological significance in soils

Abstract

Bacteria can regulate cell morphology in response to environmental conditions, altering their physiological and metabolic characteristics to improve survival. Conditional filamentation, in which cells suspend division while continuing lateral growth, is a strategy with a range of adaptive benefits. Here, we review the causes and consequences of conditional filamentation with respect to bacterial physiology, ecology and evolution. We describe four major benefits from conditional filamentation: stress tolerance, surface colonization, gradient spanning and the facilitation of biotic interactions. Adopting a filamentous growth habit involves fitness trade-offs which are also examined. We focus on the role of conditional filamentation in soil habitats, where filamentous morphotypes are highly prevalent and where environmental heterogeneity can benefit a conditional response. To illustrate the use of information presented in our review, we tested the conditions regulating filamentation by the forest soil isolate Paraburkholderia elongata 5N T . Filamentation by P. elongata was induced at elevated phosphate concentrations, and was associated with the accumulation of intracellular polyphosphate, highlighting the role of filamentation in a phosphate-solubilizing bacterium. Conditional filamentation enables bacteria to optimize their growth and metabolism in environments that are highly variable, a trait that can impact succession, symbioses, and biogeochemistry in soil environments.

The transcriptional state and chromatin landscape of cichlid jaw shape variation across species and environments

“…In addition, cichlids have long been a model of phenotypic plasticity (Meyer 1987;Wimberger 1991;Huysseune 1995;Machado-Schiaffino et al, 2014;Schneider et al, 2014;Meuthen et al, 2018;Navon et al, 2020), which is defined as the ability of a single genotype to produce a range of phenotypes in response to environmental inputs. Plasticity is critical for organismal survival in an era of rapid environmental change (Willis et al, 2008;Sih et al, 2011;Gugger et al, 2015;Karasz et al, 2022;Morgan et al, 2022). It can also influence the direction and/or speed of future evolutionary change by exposing new phenotypic and genetic variants to natural selection (Ledon-Rettig et al, 2010 ProcB;McGuigan et al, 2011 evol;Landy et al, 2020 PNAS;Campbell et al, 2021).…”

Shear-enhanced sorting of ovoid and filamentous bacterial cells using pinch flow fractionation

“…3 Filamentation is also prevalent in soil bacteria to promote mutualistic interactions between bacteria and nutrient uptake in heterogeneous soil environments. 5 Sorting of these elongated cells from the rest of the population will facilitate the study of the mechanisms behind these phenotypes and give more insight into population heterogeneity. Notably, coupling cell sorting from infectious samples with phenotypic characterization and RNA-sequencing techniques can give interesting insights into the virulence of important pathogens.…”

“…1 One such phenotype is cell filamentation, a naturally occurring phenomenon in response to stress but also a fitness strategy to prevent phagocytosis by predators, optimize colonization of a niche, and facilitate symbiotic interactions. 2–5 Size and shape-based sorting can therefore be applied in the study of filamentation in contexts where only a subpopulation of microorganisms is filamentous.…”

Antibiotic heteroresistance generated by multi-copy plasmids

“…86,87 This stress response is also known to increase genetic variation 88 by promoting bacterial mutagenesis 89,90 and enabling the horizontal transmission of virulence factors 91 and antibiotic resistance genes. 92 The SOS system also produces bacterial filaments, which have been shown to be an adaptive trait with many benefits, 58 including the promotion of tissue colonization 93 and increased tolerance to cell wall damage produced by the antibiotics used in this study. 64,94 Our study, combined with previous reports, shows that having a phenotypically diverse population is an effective adaptive strategy to survive fluctuating environmental conditions.…”

“…Note that shortly after being exposed to the antibiotic, some cells ceased dividing but continued to grow, thus producing filaments (see also Figure 4E). Conditional filamentation can be triggered by multiple molecular mechanisms, 58 including a general stress response -the SOS regulatory network -that regulates the expression of over 50 genes involved in DNA repair, DNA damage tolerance, and the induction of a DNA damage checkpoint that transiently suppresses cell division. 59 In particular, the SOS response can be triggered by the binding of β -lactamase molecules to penicillinbinding protein 3 (PBP3).…”