Many roads lead to Rome: Neutral phenotypes in microorganisms

Abstract

John Bonner pointed out that microorganisms differ in several ways, some of which may reflect neutral phenotypic evolution. For making his case, Bonner referred to interspecies differences and morphological traits. Here we consider intraspecies differences and physiological traits. As a case‐study, we examine the production of an extracellular cyclic 3 falseprefix′,5 falseprefix′ monophosphate phosphodiesterase in the cellular slime mold Dictyostelium discoideum. Temporal profiles of phosphodiesterase activity differ significantly between wild‐type strains. From that we argue that the inference drawn initially from studies on a single wild‐type, namely that the profile displayed by it pointed to an adaptive role, was mistaken. We generalize the conclusion to suggest that physiological differences exhibited by microorganisms of the same species may, but need not, reflect adaptations to different environments. Rather, the differences could be related to the fact that microorganisms live in groups whose composition can vary between homogeneous (clonal) and heterogeneous (polyclonal). More than one physiological profile is consistent with the normal development of the group in a given environment; the alternatives are neutral. When studying microbial physiology and behavior, it is expected that the observations are made on a clonal population; genetic (and so phenotypic) heterogeneity is carefully guarded against. As the example from D. discoideum shows, an unintended consequence of overlooking phenotypic heterogeneity is that one can fall into the trap of accepting a seemingly plausible, but possibly erroneous, adaptive explanation for a “normal” wild‐type phenotype.

Single-cell phenotypic plasticity modulates social behavior in Dictyostelium discoideum

“…In particular, the prediction that “cheaters” have a long-term advantage could be upended if short-term measures of reproductive success do not carry over to successive generations, so that relevant variation is effectively neutral. 2 , 62 , 68 Our results point to a role of unpredictable variation that may be much larger than previously considered when associating a genotype to a social behavior. Single-cell properties at the moment of aggregation and the derived biases are not only shaped by the genetic identity of a strain, but also by factors that are not under direct genetic control.…”

Uncovering the complexity of childhood undernutrition through strain-level analysis of the gut microbiome

“…Numerous studies have investigated the gut microbiome in undernourished children to gain insight into the potential links between gut microbiota and undernutrition. However, these studies often overlook the strain-level diversity within bacterial species, which could provide additional information on the functional roles of specific bacterial strains in the pathogenesis of undernutrition [ 24 , 25 ]. Our study addresses this gap in knowledge by analyzing the strain-level diversity of the gut microbiome in undernourished children and identifying specific strains that are differentially enriched between undernourished and healthy control children.…”

Single-cell phenotypic plasticity modulates social behaviour inDictyostelium discoideum

“…However, their underpinning and the way they get transmitted along the multicellular cycle are important to understand the evolution of social behaviours. In particular, the prediction that ‘cheaters’ have a long-term advantage could be upended if short-term measures of repro-ductive success do not carry over to successive generations, so that relevant variation is effectively neutral (Arias Del Angel et al, 2020; Nanjundiah, 2019; Forget et al, 2021). Our results point to a role of unpredictable variation that may be much larger than previously considered when associating a genotype to a social behaviour.…”