Seed Banks Alter the Rate and Direction of Molecular Evolution in Bacillus subtilis

Fluctuations in the availability of resources constrains the growth and reproduction of individuals, which in turn effects the evolution of their respective populations. Many organisms are able to respond to fluctuations by entering a reversible state of reduced metabolic activity, a phenomenon known as dormancy. This pool of dormant individuals (i.e., a seed bank) does not reproduce and is expected to act as an evolutionary buffer, though it is difficult to observe this effect directly over an extended evolutionary timescale. Through genetic manipulation, we analyze the molecular evolutionary dynamics of Bacillus subtilis populations in the presence and absence of a seed bank over 700 days. We find that the ability to enter a dormant state increases the accumulation of genetic diversity over time and alters the trajectory of mutations, findings that are recapitulated using simulations based on a simple mathematical model. While the ability to form a seed bank does not alter the degree of negative selection, we find that it consistently alters the direction of molecular evolution across genes. Together, these results show that the ability to form a seed bank affects the direction and rate of molecular evolution over an extended evolutionary timescale.

Molecular evolutionary dynamics of energy limited microorganisms

Microorganisms have the unique ability to survive extended periods of time in environments with extremely low levels of exploitable energy. To determine the extent that energy limitation affects microbial evolution, we examined the molecular evolutionary dynamics of a phylogenetically diverse set of taxa over the course of 1,000-days. We found that periodic exposure to energy limitation affected the rate of molecular evolution, the accumulation of genetic diversity, and the rate of extinction. We then determined the degree that energy limitation affected the spectrum of mutations as well as the direction of evolution at the gene level. Our results suggest that the initial depletion of energy altered the direction and rate of molecular evolution within each taxon, though after the initial depletion the rate and direction did not substantially change. However, this consistent pattern became diminished when comparisons were performed across phylogenetically distant taxa, suggesting that while the dynamics of molecular evolution under energy limitation are highly generalizable across the microbial tree of life, the targets of adaptation are specific to a given taxon.

Higher temperatures worsen the effects of mutations on protein stability

Understanding whether and how temperature increases alter the effects of mutations on protein stability is crucial for understanding the limits to thermal adaptation by organisms. Currently, it is generally assumed that the stability effects of mutations are independent of temperature. Yet, mutations should become increasingly destabilizing as temperature rises due to the increase in the energy of atoms. Here, by performing an extensive computational analysis on the essential enzyme adenylate kinase in prokaryotes, we show, for the first time, that mutations become more destabilizing with temperature both across and within species. Consistent with these findings, we find that substitution rates of prokaryotes decrease nonlinearly with temperature. Our results suggest that life on Earth likely originated in a moderately thermophilic and thermally fluctuating environment, and indicate that global warming should decrease the per-generation rate of molecular evolution of prokaryotes.

RuBisCO adaptation is more limited by phylogenetic constraint than by catalytic trade-off in plants

RuBisCO assimilates CO2 to form the sugars that fuel life on earth. Correlations between RuBisCO kinetic traits across species have led to the proposition that RuBisCO adaptation is constrained by catalytic trade-offs. However, these analyses did not consider the phylogenetic context of the enzymes that were analysed. Thus, it is possible that the observed correlations between RuBisCO kinetic traits are an artefact of the presence of phylogenetic signal in RuBisCO kinetics and the phylogenetic relationship between the species that were sampled. Here, we conducted a phylogenetically resolved analysis of RuBisCO kinetics and show that there is significant phylogenetic signal in all carboxylase kinetic traits, and significant phylogenetic signal in the Michaelis constant for O2 in species that conduct C3 photosynthesis. When accounting for this phylogenetic non-independence between enzymes, we show that the catalytic trade-off between carboxylase turnover and the Michaelis constant for CO2 is weak (~30 % dependency) and that the correlations between all other RuBisCO kinetic traits are either not-significant or marginal (<9 % dependency). Finally, we demonstrate that phylogenetic constraints have limited RuBisCO evolution to a greater extent than catalytic trade-offs. Thus, RuBisCO adaptation in angiosperms is predominantly limited by phylogenetic constraint (most likely caused by a slow rate of molecular evolution) and a partial trade-off between carboxylase turnover and the Michaelis constant for CO2.

Disentangling biological and analytical factors that give rise to outlier genes in phylogenomic matrices

The genomic data revolution has enabled biologists to develop innovative ways to infer key episodes in the history of life. Whether genome-scale data will eventually resolve all branches of the Tree of Life remains uncertain. However, through novel means of interrogating data, some explanations for why evolutionary relationships remain recalcitrant are emerging. Here, we provide four biological and analytical factors that explain why certain genes may exhibit “outlier” behavior, namely, rate of molecular evolution, alignment length, misidentified orthology, and errors in modeling. Using empirical and simulated data we show how excluding genes based on their likelihood or inferring processes from the topology they support in a supermatrix can mislead biological inference of conflict. We next show alignment length accounts for the high influence of two genes reported in empirical datasets. Finally, we also reiterate the impact misidentified orthology and short alignments have on likelihoods in large scale phylogenetics. We suggest that researchers should systematically investigate and describe the source of influential genes, as opposed to discarding them as outliers. Disentangling whether analytical or biological factors are the source of outliers will help uncover new patterns and processes that are shaping the Tree of Life.

Comparative Plastome Analysis of Root- and Stem-Feeding Parasites of Santalales Untangle the Footprints of Feeding Mode and Lifestyle Transitions

In plants, parasitism triggers the reductive evolution of plastid genomes (plastomes). To disentangle the molecular evolutionary associations between feeding on other plants below- or aboveground and general transitions from facultative to obligate parasitism, we analyzed 34 complete plastomes of autotrophic, root- and stem-feeding hemiparasitic, and holoparasitic Santalales. We observed inexplicable losses of housekeeping genes and tRNAs in hemiparasites and dramatic genomic reconfiguration in holoparasitic Balanophoraceae, whose plastomes have exceptionally low GC contents. Genomic changes are related primarily to the evolution of hemi- or holoparasitism, whereas the transition from a root- to a stem-feeding mode plays no major role. In contrast, the rate of molecular evolution accelerates in a stepwise manner from autotrophs to root- and then stem-feeding parasites. Already the ancestral transition to root-parasitism coincides with a relaxation of selection in plastomes. Another significant selectional shift in plastid genes occurs as stem-feeders evolve, suggesting that this derived form coincides with trophic specialization despite the retention of photosynthetic capacity. Parasitic Santalales fill a gap in our understanding of parasitism-associated plastome degeneration. We reveal that lifestyle-genome associations unfold interdependently over trophic specialization and feeding mode transitions, where holoparasitic Balanophoraceae provide a system for exploring the functional realms of plastomes.

Genomic signature of ongoing alkaline adaptation in a Schizothoracine fish (Cyprinidae) inhabiting soda lake on the Tibetan Plateau

Comparative genomics has elucidate the molecular footprints of adaptations to extreme environments at high altitude including hypoxia, but insight into the genomic basis of saline and alkaline adaptation in highland fish has rarely been provided. The increasing of water salinization is a growing threat to Tibetan endemic fish species. Here we performed one of the first comparative genomics studies and began to characterize genomic signature of alkaline adaptation in a Schizothoracine fish inhabiting soda lake on the Tibetan Plateau. We found that expansions of lineage-specific genes associated with ion transport and transmembrane functions, genome-wide elevated rate of molecular evolution in Schizothoracine fishes relative to other lowland teleost fish species. In addition, we found specific changes in the rate of molecular evolution between G. p. kelukehuensis and other teleost fishes for ion transport-related genes. Furthermore, we identified a set of genes associated with ion transport and energy metabolism underwent positive selection. Using tissue-transcriptomics, we found that most REGs and PSGs in G. p. kelukehuensis were broadly expressed across three tissues and significantly enriched for ion transport functions. Finally, we identified a set of ion transport-related genes with evidences for both selection and co-expressed which contributed to alkaline tolerance in G. p. kelukehuensis. Altogether, our study identified putative genomic signature and potential candidate genes contributed to ongoing alkaline adaptation in Schizothoracine fish.