Trait-trait relationships and tradeoffs vary with genome size in prokaryotes

Abstract

We report genomic traits that have been associated with the life history of prokaryotes and highlight conflicting findings concerning earlier observed trait correlations and tradeoffs. In order to address possible explanations for these contradictions we examined trait–trait variations of 11 genomic traits from ~18,000 sequenced genomes. The studied trait–trait variations suggested: (i) the predominance of two resistance and resilience-related orthogonal axes and (ii) at least in free living species with large effective population sizes whose evolution is little affected by genetic drift an overlap between a resilience axis and an oligotrophic-copiotrophic axis. These findings imply that resistance associated traits of prokaryotes are globally decoupled from resilience related traits and in the case of free-living communities also from traits associated with resource availability. However, further inspection of pairwise scatterplots showed that resistance and resilience traits tended to be positively related for genomes up to roughly five million base pairs and negatively for larger genomes. Genome size distributions differ across habitats and our findings therefore point to habitat dependent tradeoffs between resistance and resilience. This in turn may preclude a globally consistent assignment of prokaryote genomic traits to the competitor - stress-tolerator - ruderal (CSR) schema that sorts species depending on their location along disturbance and productivity gradients into three ecological strategies and may serve as an explanation for conflicting findings from earlier studies. All reviewed genomic traits featured significant phylogenetic signals and we propose that our trait table can be applied to extrapolate genomic traits from taxonomic marker genes. This will enable to empirically evaluate the assembly of these genomic traits in prokaryotic communities from different habitats and under different productivity and disturbance scenarios as predicted via the resistance-resilience framework formulated here.

The Cost of Adaptability: Resource Availability Constrains Functional Stability Under Pulsed Disturbances

“…Accordingly may nutrient limitation in some cases also select for taxa with simultaneous low resistance and low resilience. To address these conflicting observations, a recent study investigated trait-trait variations of the above highlighted genomic traits as markers for resilience and resistance from ~18,000 bacterial genomes to address trade-off between resistance and resilience traits (18). The observed trait-trait variations confirmed the hypothesized negative correlation (i.e.…”

“…In line with these expectations, previous experimental work has linked functional stability of microbial communities to the presence of generalist taxa with broad niches (17). It has been suggested that traits inferred from genomic information of microbial communities approximate life history relevant for resistance and resilience (18). For instance, genomic traits such as genome size and the fraction of transcription factors (%TF) were linked to classifications along the generalist-specialist continuum because additional auxiliary genes and regulatory capacity enhance aptness to environmental change (19,20).…”

“…resilience-related traits: RRN, generation time delineated from codon usage biases) were predicted for each ASV using the hidden state prediction option included in the PICRUSt2 software v2.4.2 (41) and using the trait values published elsewhere (18,42). CWMs of genomic trait data in each sample were computed by multiplying the predicted trait values for each ASV by its relative abundance and adding up these weighted values in each sample.…”

“…Apart from stochasticity in community re-assembly, more deterministic selection may have shaped trait distribution. Both, bacterial life history traits as well as the above highlighted resistance and resilience-related genomic features have been shown to be phylogenetically conserved (18,30). Phylogenetic distance-based community composition should accordingly reflect a greater impact of the disturbance regime compared to the purely compositional metric applied above.…”

Life history strategies and niches of soil bacteria emerge from interacting thermodynamic, biophysical, and metabolic traits

“…This is highlighted by the significant variation in growth rates observed under resource-limited conditions [8] and across broad lineages [9]. The failure of existing organizing principles to fully capture the complexity of microbial systems [10] point to important phenotypic variation in growth, and the need to understand and represent how key traits regarding resource acquisition, resource use, and stress tolerance are realized in conjunction with maximum growth potential to adapt to a particular environmental niche [11,12].…”