Evolutionary tradeoffs in cellular composition across diverse bacteria

Abstract

One of the most important classic and contemporary interests in biology is the connection between cellular composition and physiological function. Decades of research have allowed us to understand the detailed relationship between various cellular components and processes for individual species, and have uncovered common functionality across diverse species. However, there still remains the need for frameworks that can mechanistically predict the tradeoffs between cellular functions and elucidate and interpret average trends across species. Here we provide a comprehensive analysis of how cellular composition changes across the diversity of bacteria as connected with physiological function and metabolism, spanning five orders of magnitude in body size. We present an analysis of the trends with cell volume that covers shifts in genomic, protein, cellular envelope, RNA and ribosomal content. We show that trends in protein content are more complex than a simple proportionality with the overall genome size, and that the number of ribosomes is simply explained by cross-species shifts in biosynthesis requirements. Furthermore, we show that the largest and smallest bacteria are limited by physical space requirements. At the lower end of size, cell volume is dominated by DNA and protein content—the requirement for which predicts a lower limit on cell size that is in good agreement with the smallest observed bacteria. At the upper end of bacterial size, we have identified a point at which the number of ribosomes required for biosynthesis exceeds available cell volume. Between these limits we are able to discuss systematic and dramatic shifts in cellular composition. Much of our analysis is connected with the basic energetics of cells where we show that the scaling of metabolic rate is surprisingly superlinear with all cellular components.

Chromosome Translocation Inflates Bacillus Forespores and Impacts Cellular Morphology

“…To estimate average DNA radial separation d , we approximate the DNA molecule by a cylinder of the same length as a whole molecule: d 2 L DNA = V fspore , where L DNA is the total DNA length (Purohit et al, 2003). Since bp linear size is 0.34 nm (Kempes et al, 2016; Raspaud et al, 2000), we obtain that the typical distance between two neighboring DNA strands is ~8.4 nm. DNA electrostatic interactions are screened in the ionic solutions due to counterions and the typical Debye’s electrostatic screening length of about 0.8 nm (Podgornik et al, 2016; Raspaud et al, 2000).…”

Microdiversification of a Pelagic Polynucleobacter Species Is Mainly Driven by Acquisition of Genomic Islands from a Partially Interspecific Gene Pool

“…Generally, in Polynucleobacter, there seems to be strong selection pressure toward small genomes, indicated by a high fraction of coding bases and small genome sizes compared to its closest related genera (47). Diversification by GIs, i.e., the partitioning of certain functions among closely related strains, may be an elegant way to reduce competition and minimize the amount of genetic material for a single cell (69). As a consequence of such microniche partitioning, the niche space of a species can be expanded and exploited more efficiently (70).…”

Assessment of the bimodality in the distribution of bacterial genome sizes

“…A number of recent studies have focussed on the evolution of bacterial genome sizes (Kempes et al, 2016), indicating that the interaction between an organism and its ecological niche, for example, resource availability and environmental stability, selects the genome size of the species (Konstantinidis and Tiedje, 2004;Bentkowski et al, 2015). The exact mechanisms driving the genome sizes are still not fully resolved (Sabath et al, 2013, Kempes et al, 2016.…”

“…Some interesting observations with a potential link to the nature of distribution have been emerging in recent years. For example, (i) the bimodality in flow cytometric analysis of bacterial DNA content has been implicated with the bimodal genome size distribution (Schattenhofer et al, 2011;Morán et al, 2015); (ii) there may be other factors such as physical cell space constraints having a role in genome size selection (Kempes et al, 2016) and (iii) perhaps most intriguingly, numerous studies Assessment of the bimodality in the distribution of bacterial genome sizes HS Gweon et al from metagenomics are indicating that species with small genomes are more common than previously thought (Giovannoni et al, 2014;Morán et al, 2015). With the rise of single-cell genomics and improved bioinformatic assembly methods coupled with the continual reduction in genome sequencing, we are currently witnessing rapid growth in the number of sequenced genomes.…”

“…A number of recent studies have focussed on the evolution of bacterial genome sizes (Kempes et al, 2016), indicating that the interaction between an organism and its ecological niche, for example, resource availability and environmental stability, selects the genome size of the species (Konstantinidis and Tiedje, 2004;Bentkowski et al, 2015). The exact mechanisms driving the genome sizes are still not fully resolved (Sabath et al, 2013, Kempes et al, 2016. It has, however, been speculated that species living in invariant niches tend to have small genomes, as stability acts to reduce genome size due the metabolic burden of replicating DNA with no adaptive value (Giovannoni et al, 2005(Giovannoni et al, , 2014 such as in obligatory and intracellular pathogens or mutualists (Moran, 2003;Klasson and Andersson, 2004;Moya et al, 2009).…”