bioRxiv Science⌕ Search

Biology subjects

Gralka, M.

Publications and source records attributed to Gralka, M..

13 recordsLinked to original sources

Biosynthesis cost and catabolic pathway length explain frequency of amino acid utilization as carbon sources by bacteria

Heterotrophic bacteria exhibit remarkable metabolic diversity. Experimental phenotyping of individual strains is often impractical due to the diversity of metabolic strategies, highlighting the need for predictive approaches based on biochemical principles. Here, we demonstrate that bacteria preferentially catabolize amino acids that are energetically inexpensive to synthesize and require shorter degradation pathways. Our results show how general biochemical constraints shape amino acid catabolism across bacterial lineages and provide a framework for integrating microbial physiology into predictive ecological theory.

microbiology↗

Rapid resistance evolution against phage cocktails

When bacteria are treated with multiple antibiotics simultaneously, resistance is highly unlikely to evolve. In stark contrast, resistance against multiple phages frequently arises during therapy. Why does resistance against multi-phage cocktails evolve so easily? Using a mathematical model, we show how the bacterial evolutionary dynamics and phage replicative dynamics uniquely intertwine, facilitating the rapid evolution of multi-phage resistance. As different phages replicate and become inhibitory at varying time points, bacteria can sequentially acquire resistance rather than simultaneously - increasing the chance of multi-resistance by orders of magnitude. Additionally, we predict and experimentally verify a regime where multi-phage resistance is robustly prevented. Our findings provide a framework for the rational design of phage cocktails to curtail resistance development. Resistance can be minimized by reducing the dose of the most potent phages or by using phages with longer latent periods, as this helps synchronize multi-phage selection.

microbiology↗

Cross-feeding options define eco-evolutionary dynamics of deep oligotrophic groundwater microbiome

Deep groundwaters populated by diverse and active microbes are among the most energy and nutrient-limited ecosystems. Characteristics of this ecosystem including nutrient and dispersal limitations, low cell densities, and episodic growth strategy interactively underpin the so far elusive eco-evolutionary dynamics of its microbiome. Here we applied a modular metabolic analyses on genome-resolved reconstructed community of disconnected deep groundwaters in the Fennoscandian Shield. In the community of deeper groundwaters despite their highly oligotrophic nature, lineages with larger genomes maintained larger populations which we hypothesize to be connected with their limited cross-feeding options. Thus providing an extension on the streamlining theory emphasizing the importance of ecological interactions in genome evolution which is further supported by the observed decrease in abundance of lineages with known metabolic dependencies, such as Patescibacteria and DPANN, with depth. The modular metabolic analyses showed that remarkably common niches based on same cross-feeding interactions are also available in different groundwaters, in addition to common niches for primary production. While these shared niches are critical for community assembly in this ecosystem, in different boreholes different lineages populated them. Our results provided new insights into the role of metabolic cross-feeding in genome evolution and community assembly of deep groundwater microbiome.

microbiology↗

Widespread B-vitamin auxotrophy in marine particle-associated bacteria

Microbial community assembly is governed by trophic interactions that mediate the transfer of carbon sources and biomass building blocks between species. However, central metabolism corresponds to only a small fraction of the biosynthetic potential of microbes: metabolites such as antimicrobial compounds, signaling molecules, and co-factors are underexplored forces shaping microbial communities. Here, we focus on B vitamin exchange in coastal marine bacterial communities that degrade particulate organic matter and find that natural seawater communities are vitamin limited. While almost a third of bacterial isolates from these communities are B vitamin auxotrophs, the pioneering degraders that first arrive on particles are vitamin producers that likely support auxotrophs through cross-feeding. However, combining experiments and a resource-explicit model, we show that auxotroph growth is often not restored by coculture with vitamin producers, but rather requires lysis and subsequent vitamin recycling. Our results highlight the importance of vitamin auxotrophies and lysis-mediated cross-feeding as important factors controlling microbial community assembly and succession on marine particles.

microbiology↗

Fundamental metabolic strategies of heterotrophic bacteria

Through their metabolism, heterotrophic microbes drive carbon cycling in many environments (1). These microbes consume (and produce) hundreds to thousands of different metabolic substrates, begging the question of what level of description is required to understand the metabolic processes structuring their communities: do we need to account for the detailed metabolic capabilities of each organism, or can these capabilities be understood in terms of a few well-conserved carbon utilization strategies that could be more easily interpreted and more robustly predicted? Based on the high-throughput phenotyping of a diverse collection of marine bacteria, we showed that the fundamental metabolic strategy of heterotrophic microbes can be understood in terms of a single axis of variation, representing their preference for either glycolytic (sugars) or gluconeogenic (amino and organic acids) carbon sources. Moreover, an organisms position on this axis is imprinted in its genome, allowing us to successfully predict metabolic strategy across the bacterial tree of life. Our analysis also unveils a novel and general association between metabolic strategy and genomic GC content, which we hypothesize results from the difference in C:N supply associated with typical sugar and acid substrates. Thus, our work reveals a fundamental constraint on microbial evolution that structures bacterial genomes and communities and can be leveraged to understand diversity in functional terms, beyond catalogs of genes and taxa.

microbiology↗

A Genome-Scale Metabolic Model of Marine Heterotroph Vibrio splendidus sp. 1A01

While the Vibrio splendidus species is best known as an opportunistic pathogen in oysters, the Vibrio splendidus sp. 1A01 strain was first identified as an early colonizer of synthetic chitin particles incubated in seawater. To gain a better understanding of its metabolism, a genome-scale metabolic model (GSMM) of V. splendidus sp. 1A01 was reconstructed. GSMMs enable us to simulate all metabolic reactions in a bacterial cell using Flux Balance Analysis. A draft model was built using an automated pipeline from BioCyc. Manual curation was then performed based on experimental data, in part by gap-filling metabolic pathways and tailoring the models biomass reaction to V. splendidus sp. 1A01. The challenges of building a metabolic model for a marine microorganism like V. splendidus sp. 1A01 are described.

microbiology↗

Viral infection switches the balance between bacterial and eukaryotic recyclers of organic matter during algal blooms

Algal blooms are hotspots of marine primary production and play central roles in microbial ecology and global nutrient cycling. When blooms collapse, organic carbon is transferred to higher trophic levels, microbial respiration or sinking in proportions that depend on the dominant mortality agent. Viral infection can lead to bloom termination, but its impact on the fate of carbon remains an open question. Here, we characterized the consequences of viral infection on the microbiome composition and biogeochemical landscape of marine ecosystems by conducting a large-scale mesocosm experiment. Moniroting of seven induced coccolithophore blooms, which showed different degrees of viral infection, revealed that only high levels of viral infection caused significant shifts in the composition of free-living bacterial and eukaryotic assemblages. Intriguingly, viral infection favored the growth of eukaryotic heterotrophs (thraustochytrids) over bacteria as potential recyclers of organic matter. By combining modeling and quantification of active viral infection at a single-cell resolution, we estimate that viral infection can increase per-cell rates of extracellular carbon release by 2-4.5 fold. This happened via production of acidic polysaccharides and particulate inorganic carbon, two major contributors to carbon sinking into the deep ocean. These results reveal the impact of viral infection on the fate of carbon through microbial recyclers of organic matter in large-scale coccolithophore blooms.

microbiology↗

Public good exploitation in natural bacterioplankton communities

Microorganisms such as bacteria often interact with their environment through extracellular molecules that increase access to limiting resources. These secretions can act as public goods, creating incentives for exploiters, a.k.a cheaters, to invade and steal public goods away from producers. This phenomenon has been studied extensively in microbiology due to its implications for the evolution of cooperation, but little is known about the occurrence and impact of public good exploiters in the environment. Here, we develop a new genomic approach to systematically identify bacteria that can exploit public goods produced during the degradation of polysaccharides. Focusing on chitin - the second most abundant biopolymer on the planet, we show that public good exploiters are active in natural marine microbial communities that assemble on chitin particles, invading during early stages of colonization and potentially hindering degradation. Unlike in classical studies of social evolution, exploiters and polysaccharide degraders are not isogenic and instead belong to distant lineages, facilitating their coexistence. Our approach opens novel avenues to use the wealth of genomic data available to infer ecological roles and interactions among microbes.

microbiology↗

The mutability of demographic noise in microbial range expansions

Demographic noise, the change in the composition of a population due to random birth and death events, is an important driving force in evolution because it reduces the efficacy of natural selection. Demographic noise is typically thought to be set by the population size and the environment, but recent experiments with microbial range expansions have revealed substantial strain-level differences in demographic noise under the same growth conditions. Many genetic and phenotypic differences exist between strains; to what extent do single mutations change the strength of demographic noise? To investigate this question, we developed a high-throughput method for measuring demographic noise in colonies without the need for genetic manipulation. By applying this method to 191 randomly-selected single gene deletion strains from the E. coli Keio collection, we find that a typical single gene deletion mutation decreases demographic noise by 8% (maximal decrease: 81%). We find that the strength of demographic noise is an emergent trait at the population level that can be predicted by colony-level traits but not cell-level traits. The observed differences in demographic noise from single gene deletions can increase the establishment probability of beneficial mutations by almost an order of magnitude higher than the wild type. Our results show that single mutations can substantially alter adaptation through their effects on demographic noise and suggest that demographic noise can be an evolvable phenotype of a population.

evolutionary biology↗

Context-dependent dynamics lead to the assembly of functionally distinct pitcher-plant microbiomes

Niche construction through interspecific interactions can condition future community states on past ones. However, the extent to which such history dependency can steer communities towards functionally different states remains a subject of active debate. Using bacterial communities collected from wild pitchers of the carnivorous pitcher plant, Sarracenia purpurea, we tested the effects of history on composition and function across communities assembled in synthetic pitcher plant microcosms. We found that the diversity of assembled communities was determined by the diversity of the system at early, pre-assembly stages. Species composition was also contingent on early community states, not only because of differences in the species pool, but also because the same species had different dynamics in different community contexts. Importantly, compositional differences were proportional to differences in function, as profiles of resource use were strongly correlated with composition, despite convergence in respiration rates. Early differences in community structure can thus propagate to mature communities, conditioning their functional repertoire.

ecology↗

Environmental disorder can tip the population genetics of range expansions

Evolutionary dynamics is fundamentally shaped by stochastic processes: spon-taneous mutations enter populations randomly, and the fate of a mutant lineage is determined by the competition between (random) genetic drift and (determin-istic) selection. In populations undergoing range expansions, fluctuations in the reproductive process and the local motion of individuals are enhanced within a small subpopulation at the edge of the population. Range expansions are typically studied in homogeneous environments, but we argue here that the fluctuations at the range edge are susceptible to small-scale environmental heterogeneities that may have a strong effect on the evolutionary dynamics of the expanding population.\n\nTo show this, we tracked the dynamics of the clones of spontaneous mutations with a tunable fitness effect in bacterial colonies grown on randomly disordered surfaces. We find that environmental heterogeneity on scales much larger than an individual, but much smaller than the total population, can dramatically reduce the efficacy of selection. Time lapse microscopy and computer simulations suggest that this effect is a general consequence of a local \"pinning\" of the expansion front, whereby stretches of the front are slowed down on a length scale that depends on the structure of the environmental heterogeneity. This pinning focuses the range expansion into a small number of individuals with access to expansion paths, increasing the importance of chance and thus limiting the efficacy of selection.

evolutionary biology↗

Collective motion conceals fitness differences in crowded cellular populations

Many cellular populations are tightly-packed, for example microbial colonies and biofilms [39, 10, 41], or tissues and tumors in multi-cellular organisms [11, 29]. Movement of one cell inside such crowded assemblages requires movement of others, so that cell displacements are correlated over many cell diameters [28, 6, 31]. Whenever movement is important for survival or growth [15, 34, 38, 9], such correlated rearrangements could couple the evolutionary fate of different lineages. Yet, little is known about the interplay between mechanical stresses and evolution in dense cellular populations. Here, by tracking deleterious mutations at the expanding edge of yeast colonies, we show that crowding-induced collective motion prevents costly mutations from being weeded out rapidly. Joint pushing by neighboring cells generates correlated movements that suppress the differential displacements required for selection to act. Such mechanical screening of fitness differences allows the mutants to leave more descendants than expected under non-mechanical models, thereby increasing their chance for evolutionary rescue [2, 5]. Our work suggests that mechanical interactions generally influence evolutionary outcomes in crowded cellular populations, which has to be considered when modeling drug resistance or cancer evolution [1, 22, 34, 30, 36, 42].

biophysics↗

Mechanical interactions in bacterial colonies and the surfing probability of beneficial mutations

Bacterial conglomerates such as biofilms and microcolonies are ubiquitous in nature and play an important role in industry and medicine. In contrast to well-mixed, diluted cultures routinely used in microbial research, bacteria in a microcolonv interact mechanically with one another and with the substrate to which they are attached. Despite their ubiquity, little is known about the role of such mechanical interactions on growth and biological evolution of microbial populations. Here we use a computer model of a microbial colony of rod-shaped cells to investigate how physical interactions between cells determine their motion in the colony, this affects biological evolution. We show that the probability that a faster-growing mutant \"surfs\" at the colonys frontier and creates a macroscopic sector depends on physical properties of cells (shape, elasticity, friction). Although all these factors contribute to the surfing probability in seemingly different ways, they all ultimately exhibit their effects by altering the roughness of the expanding frontier of the colony and the orientation of cells. Our predictions are confirmed by experiments in which we measure the surfing probability for colonies of different front roughness. Our results show that physical interactions between bacterial cells play an important role in biological evolution of new traits, and suggest that these interaction may be relevant to processes such as de novo evolution of antibiotic resistance.

evolutionary biology↗