Toward quantifying the adaptive role of bacterial pangenomes during environmental perturbations

Abstract

Metagenomic surveys have revealed that natural microbial communities are predominantly composed of sequence-discrete, species-like populations but the genetic and/or ecological processes that maintain such populations remain speculative, limiting our understanding of population speciation and adaptation to perturbations. To address this knowledge gap, we sequenced 112 Salinibacter ruber isolates and 12 companion metagenomes from four adjacent saltern ponds in Mallorca, Spain that were experimentally manipulated to dramatically alter salinity and light intensity, the two major drivers of this ecosystem. Our analyses showed that the pangenome of the local Sal. ruber population is open and similar in size (~15,000 genes) to that of randomly sampled Escherichia coli genomes. While most of the accessory (noncore) genes were isolate-specific and showed low in situ abundances based on the metagenomes compared to the core genes, indicating that they were functionally unimportant and/or transient, 3.5% of them became abundant when salinity (but not light) conditions changed and encoded for functions related to osmoregulation. Nonetheless, the ecological advantage of these genes, while significant, was apparently not strong enough to purge diversity within the population. Collectively, our results provide an explanation for how this immense intrapopulation gene diversity is maintained, which has implications for the prokaryotic species concept.

Towards estimating the number of strains that make up a natural bacterial population

“…Samples CM, DZ, and UM yielded only isolates that each was assigned to a different CV and were not used for the subsampling calculations. Samples and isolates recovered from the Mallorca solar salterns are named according to the different ponds: control (C), dilution (D), and unshaded (U) at three time points: time-zero (Z), 1-week (W), and 1-month (M) (e.g., sample "UM" denotes Unshaded at 1 month) (22). The sample and isolates from Fuerteventura area denoted by "FV" in the name.…”

Pangenome Evolution in Environmentally Transmitted Symbionts of Deep-Sea Mussels Is Governed by Vertical Inheritance

“…The core genes in a pangenome are present in each individual while the remaining genes are considered accessory ( Brockhurst et al 2019 ). Pangenome size and structure vary across bacterial species ( Maistrenko et al 2020 ), and pangenomic diversity is important for bacterial adaptation in environmental species, where accessory genes are often niche-specific ( Kashtan et al 2014 ; Liao et al 2021 ; Conrad et al 2022 ). To understand microbial adaptation, it is thus crucial to understand the evolutionary processes that shape pangenome diversity.…”

RecruitPlotEasy: An Advanced Read Recruitment Plot Tool for Assessing Metagenomic Population Abundance and Genetic Diversity

“…This discovery is also important in medical microbiology; for instance, in identifying which population is the causative agent of disease ( Pena-Gonzalez et al, 2019 ). More recent work has even shown that intermediate identity genotypes, for example, sharing 85–95% ANI, when present, are ecologically differentiated and thus, should probably be considered distinct species ( Conrad et al, 2021 ; Rodriguez-R et al, 2021 ), rather than representing cultivation (or other sampling) biases ( Murray et al, 2021 ).…”