Growth rate evolution in improved environments under Prodigal Son dynamics.
ABSTRACT: I use an individual-based model to investigate the evolution of cell division rates in asexual populations under chronic environmental enrichment. I show that maintaining increased growth rates over hundreds of generations following environmental improvement can be limited by increases in cellular damage associated with more rapid reproduction. In the absence of further evolution to either increase damage tolerance or decrease the cost of repair or rate of damage, environmental improvement does not reliably lead to long-term increases in reproductive rate in microbes. Here, more rapid cell division rates also increases damage, leading to selection for damage avoidance or repair, and a subsequent decrease in population growth, which I call Prodigal Son dynamics, because the consequences of 'living fast' force a return to ancestral growth rates. Understanding the conditions under which environmental enrichment is expected to sustainably increase cell division rates is important in applications that require rapid cell division (e.g. biofuel reactors) or seek to avoid the emergence of rapid cell division rates (controlling biofouling).
Project description:Because of their large population sizes and rapid cell division rates, marine microbes have, or can generate, ample variation to fuel evolution over a few weeks or months, and subsequently have the potential to evolve in response to global change. Here we measure evolution in the marine diatom Skeletonema marinoi evolved in a natural plankton community in CO2-enriched mesocosms deployed in situ. Mesocosm enclosures are typically used to study how the species composition and biogeochemistry of marine communities respond to environmental shifts, but have not been used for experimental evolution to date. Using this approach, we detect a large evolutionary response to CO2 enrichment in a focal marine diatom, where population growth rate increased by 1.3-fold in high CO2-evolved lineages. This study opens an exciting new possibility of carrying out in situ evolution experiments to understand how marine microbial communities evolve in response to environmental change.
Project description:Cell size is a complex trait, derived from both genetic and environmental factors. Environmental determinants of bacterial cell size identified to date primarily target assembly of cytosolic components of the cell division machinery. Whether certain environmental cues also impact cell size through changes in the assembly or activity of extracytoplasmic division proteins remains an open question. Here, we identify extracellular pH as a modulator of cell division and a significant determinant of cell size across evolutionarily distant bacterial species. In the Gram-negative model organism Escherichia coli, our data indicate environmental pH impacts the length at which cells divide by altering the ability of the terminal cell division protein FtsN to localize to the cytokinetic ring where it activates division. Acidic environments lead to enrichment of FtsN at the septum and activation of division at a reduced cell length. Alkaline pH inhibits FtsN localization and suppresses division activation. Altogether, our work reveals a previously unappreciated role for pH in bacterial cell size control.
Project description:BACKGROUND: The quality of automated gene prediction in microbial organisms has improved steadily over the past decade, but there is still room for improvement. Increasing the number of correct identifications, both of genes and of the translation initiation sites for each gene, and reducing the overall number of false positives, are all desirable goals. RESULTS: With our years of experience in manually curating genomes for the Joint Genome Institute, we developed a new gene prediction algorithm called Prodigal (PROkaryotic DYnamic programming Gene-finding ALgorithm). With Prodigal, we focused specifically on the three goals of improved gene structure prediction, improved translation initiation site recognition, and reduced false positives. We compared the results of Prodigal to existing gene-finding methods to demonstrate that it met each of these objectives. CONCLUSION: We built a fast, lightweight, open source gene prediction program called Prodigal http://compbio.ornl.gov/prodigal/. Prodigal achieved good results compared to existing methods, and we believe it will be a valuable asset to automated microbial annotation pipelines.
Project description:A bioinformatics and experimental study about the cell wall in bacteria of Planctomycetes phylum. Bacteria of Planctomycetes phylum show unique cell division processes and are able to engulf large molecules and one species is even able to egulf other bacteria. Due to such unique abilites and lack of genes for peptidoglycan, it has been a topic of debate whether these bacteria do or do not have the usual bacterial cell wall formed by peptidoglycan polymers. Here we have provided a data set of the protein fasta files of the genomes used for the comparative analysis in the study. The gene prediction of the older genomes were redone using prodigal to get a consistent and reliable gene prediction quality. Here we have uploaded the fasta files with newly predicted protein sequences and new protein IDs for each genome.
Project description:Replicative aging has been demonstrated in asymmetrically dividing unicellular organisms, seemingly caused by unequal damage partitioning. Although asymmetric segregation and inheritance of potential aging factors also occur in symmetrically dividing species, it nevertheless remains controversial whether this results in aging. Based on large-scale single-cell lineage data obtained by time-lapse microscopy with a microfluidic device, in this report, we demonstrate the absence of replicative aging in old-pole cell lineages of Schizosaccharomyces pombe cultured under constant favorable conditions. By monitoring more than 1,500 cell lineages in 7 different culture conditions, we showed that both cell division and death rates are remarkably constant for at least 50-80 generations. Our measurements revealed that the death rate per cellular generation increases with the division rate, pointing to a physiological trade-off with fast growth under balanced growth conditions. We also observed the formation and inheritance of Hsp104-associated protein aggregates, which are a potential aging factor in old-pole cell lineages, and found that these aggregates exhibited a tendency to preferentially remain at the old poles for several generations. However, the aggregates were eventually segregated from old-pole cells upon cell division and probabilistically allocated to new-pole cells. We found that cell deaths were typically preceded by sudden acceleration of protein aggregation; thus, a relatively large amount of protein aggregates existed at the very ends of the dead cell lineages. Our lineage tracking analyses, however, revealed that the quantity and inheritance of protein aggregates increased neither cellular generation time nor cell death initiation rates. Furthermore, our results demonstrated that unusually large amounts of protein aggregates induced by oxidative stress exposure did not result in aging; old-pole cells resumed normal growth upon stress removal, despite the fact that most of them inherited significant quantities of aggregates. These results collectively indicate that protein aggregates are not a major determinant of triggering cell death in S. pombe and thus cannot be an appropriate molecular marker or index for replicative aging under both favorable and stressful environmental conditions.
Project description:DNA damage checkpoints exist to promote cell survival and the faithful inheritance of genetic information. It is thought that one function of such checkpoints is to ensure that cell division does not occur before DNA damage is repaired. However, in unicellular organisms, rapid cell multiplication confers a powerful selective advantage, leading to a dilemma. Is the activation of a DNA damage checkpoint compatible with rapid cell multiplication? By uncoupling the initiation of DNA replication from cell division, the Escherichia coli cell cycle offers a solution to this dilemma. Here, we show that a DNA double-strand break, which occurs once per replication cycle, induces the SOS response. This SOS induction is needed for cell survival due to a requirement for an elevated level of expression of the RecA protein. Cell division is delayed, leading to an increase in average cell length but with no detectable consequence on mutagenesis and little effect on growth rate and viability. The increase in cell length caused by chronic DNA double-strand break repair comprises three components: two types of increase in the unit cell size, one independent of SfiA and SlmA, the other dependent of the presence of SfiA and the absence of SlmA, and a filamentation component that is dependent on the presence of either SfiA or SlmA. These results imply that chronic checkpoint induction in E. coli is compatible with rapid cell multiplication. Therefore, under conditions of chronic low-level DNA damage, the SOS checkpoint operates seamlessly in a cell cycle where the initiation of DNA replication is uncoupled from cell division.
Project description:Rapid response to environmental changes is achieved by uni- and multicellular organisms through a series of molecular events, often involving modification of macromolecules, including proteins, nucleic acids and lipids. Amongst these, ADP-ribosylation is of emerging interest because of its ability to modify different macromolecules in the cells, and its association with many key biological processes, such as DNA-damage repair, DNA replication, transcription, cell division, signal transduction, stress and infection responses, microbial pathogenicity and aging. In this review, we provide an update on novel pathways and mechanisms regulated by ADP-ribosylation in organisms coming from all kingdoms of life.
Project description:Filamentous organisms represent an example where incomplete separation after cell division underlies the development of multicellular formations. With a view to understanding the evolution of more complex multicellular structures, we explore the transition of multicellular growth from one to two dimensions. We develop a computational model to simulate multicellular development in populations where cells exhibit density-dependent division and death rates. In both the one- and two-dimensional contexts, multicellular formations go through a developmental cycle of growth and subsequent decay. However, the model shows that a transition to a higher dimension increases the size of multicellular formations and facilitates the maintenance of large cell clusters for significantly longer periods of time. We further show that the turnover rate for cell division and death scales with the number of iterations required to reach the stationary multicellular size at equilibrium. Although size and life cycles of multicellular organisms are affected by other environmental and genetic factors, the model presented here evaluates the extent to which the transition of multicellular growth from one to two dimensions contributes to the maintenance of multicellular structures during development.
Project description:Background:Characterizing the behaviors of dynamic systems requires capturing them with high temporal and spatial resolution. Owing to its transparency and genetic tractability, the Arabidopsis thaliana root lends itself well to live imaging when combined with cell and tissue-specific fluorescent reporters. We developed a novel 4D imaging method that utilizes simple confocal microscopy and readily available components to track cell divisions in the root stem cell niche and surrounding region for up to 1 week. Results:Using this method, we performed a direct measurement of cell division intervals within and around the root stem cell niche. The results reveal a short, steep gradient of cell division rates in proximal stem cells, with progressively more rapid cell division rates from quiescent center (QC), to cells in direct contact with the QC (initials), to their immediate daughters, after which division rates appear to become more homogeneous. Conclusions:These results provide a baseline to study how perturbations in signaling could affect cell division patterns in the root meristem. This new setup further allows us to finely analyze meristematic cell division rates that lead to patterning.
Project description:Under global change, populations have four possible responses: 'migrate, acclimate, adapt or die' (Gienapp et al. 2008 Climate change and evolution: disentangling environmental and genetic response. Mol. Ecol. 17, 167-178. (doi:10.1111/j.1365-294X.2007.03413.x)). The challenge is to predict how much migration, acclimatization or adaptation populations are capable of. We have previously shown that populations from more variable environments are more plastic (Schaum et al. 2013 Variation in plastic responses of a globally distributed picoplankton species to ocean acidification. Nature 3, 298-230. (doi:10.1038/nclimate1774)), and here we use experimental evolution with a marine microbe to learn that plastic responses predict the extent of adaptation in the face of elevated partial pressure of CO2 (pCO2). Specifically, plastic populations evolve more, and plastic responses in traits other than growth can predict changes in growth in a marine microbe. The relationship between plasticity and evolution is strongest when populations evolve in fluctuating environments, which favour the evolution and maintenance of plasticity. Strikingly, plasticity predicts the extent, but not direction of phenotypic evolution. The plastic response to elevated pCO2 in green algae is to increase cell division rates, but the evolutionary response here is to decrease cell division rates over 400 generations until cells are dividing at the same rate their ancestors did in ambient CO2. Slow-growing cells have higher mitochondrial potential and withstand further environmental change better than faster growing cells. Based on this, we hypothesize that slow growth is adaptive under CO2 enrichment when associated with the production of higher quality daughter cells.