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Mall, A.

Publications and source records attributed to Mall, A..

7 recordsLinked to original sources

Growth rate dependent DNA methylation patterns along bacterial chromosomes

DNA methylation plays critical roles in gene regulation in bacteria, from regulating essential processes like the cell cycle to phenotypes of practical interest like pathogenicity and motility. Synthetic manipulation of global methylation levels has broad impacts on cellular physiology, changing expression patterns of hundreds of genes. However, whether or how environmental variation in natural settings similarly impacts DNA methylation patterns has been unclear. In this work, using the alphaproteobacteria Methylobacterium extorquens and Caulobacter crescentus as model systems, we discover the methylome is highly fluid in response to environmental variation, with different environments leading to distinct patterns of increased or decreased methylation levels along the chromosome. Despite a heterogeneous effect of different environments on methylation patterns, we find a general principle where the dependence of methylation states on position in the genome decreases in proportion to growth rate. A simple model that considers the methylation state through different phases of the cell cycle as a function of distance from an origin provides a framework to interpret the effects of different stressors upon the observed environmental responsiveness of the methylation patterns. Our work highlights how sequencing data alone can shed light on important aspects of microbial physiology. Significance StatementDNA methylation is known to profoundly impact gene regulation in prokaryotes, with both distinct methylation states at specific loci and global levels of DNA methylation modulating critical cellular phenotypes. Yet whether or how DNA methylation patterns depend on environmental variation remains unclear. Using Methylobacterium and Caulobacter as model systems, we combine experiments and theory to uncover general principles of how global patterns of DNA methylation are shaped by the environment. In particular, we discover a positive relationship between growth rate and the magnitude of the genomic position-dependent methylation level, highlighting how sequencing data can provide a culture-independent approach to estimating microbial traits like growth rate in natural settings. Our results resolve an open question, highlighting that DNA methylation patterns in bacteria can rapidly change in response to environmental shifts and revealing rules by which methylation patterns can help understand cellular phenotypes.

microbiology↗

Aurora vent field is a hotspot for microbial hydrogen oxidation in the Arctic Ocean

Molecular hydrogen (H2) is a widespread, energetically efficient reductant supporting microbial metabolism across most known ecosystems. Although seafloor hydrothermal vents are major energy providers for H2-oxidizing microorganisms, the diversity of H2 oxidation potential in H2-rich systems remains poorly constrained. Here, we use a metagenomic approach to, for the first time, assess the genome-resolved microbial energy conservation potential within hydrothermal deposits and sediments from the ice-covered, extraordinarily H2-rich Aurora Vent Field in the Arctic Ocean. Community-wide analysis revealed broad taxonomic representation of microorganisms with the potential to consume H2 for energy conservation. Notably, we report the first genome belonging to the cosmopolitan Zetaproteobacteria genus Mariprofundus encoding the capacity for H2 oxidation. Additionally, novel, highly abundant Aquificota at Aurora encode uptake hydrogenases not previously characterized as central to H2 oxidation at deep sea vents. The encoded gene content of abundant taxa points to a preference for flexible rather than obligate lithotrophic energy metabolism. A substantial fraction of inferred H2-oxidizing potential is associated with presumed heterotrophs, potentially enhancing carbon transfer efficiency within the Aurora microbial food web. Overall, this study sheds new light on the importance of H2 availability for shaping microbial communities in hydrothermal systems. ImportanceHydrogen oxidation is a potent energy source for microorganisms that contributes to shaping and sustaining food webs in marine and terrestrial habitats, with particular importance in deep-sea chemosynthetic communities. This study provides detailed insights into how exceptionally high hydrogen availability at the Aurora Vent Field may influence microbial community structure, revealing that hydrogen oxidation potential is widespread among diverse, metabolically versatile taxa rather than obligate hydrogen oxidizers. Our findings refine current understanding of microbial energy flow and carbon cycling in hydrogen-rich hydrothermal systems. These results inform future efforts to model microbial food webs, predict ecosystem responses to changing geochemical conditions, and explore metabolic interactions in deep-sea chemosynthetic habitats more broadly.

microbiology↗

Evolution uncovers a general tradeoff between recovery after heat shock and growth at elevated temperatures

The maintenance of microbial diversity depends upon fitness tradeoffs between environments. While the importance of tradeoffs is clear, it has been surprisingly difficult to predict which traits they will occur between and at how granular a level. For example, it is unclear whether performance between a constant versus a pulsed exposure of the same stress tend to be positively correlated, independent of each other, or negatively correlated. Empirically, it has been shown that a critical feature structuring environments is temperature. However, the compatibility between strategies to deal with different forms of heat stress is unclear. For instance, are strains that grow well at higher temperatures also stronger at withstanding heat shock? To understand how environmental microbes can adapt to better deal with different forms of heat stress, we performed an evolution experiment using a dominant phyllosphere microbe Methylobacterium extorquens in a regime of intermittent heat shock. We identified the genetic basis of adaptation, discovering a large number of loci capable of mediating adaptation to heat shock, most of which previously had not been linked to heat stress. Despite the genetic divergence, we discovered a general tradeoff between heat shock resistance and growth at consistently elevated temperatures. We found this tradeoff was not limited to evolved isolates, but was also represented across a sample of environmentally isolated Methylobacterium strains. These findings indicate a generic conflict between strategies to deal with heat shock recovery and growth at elevated temperatures, suggesting even variation in intensities of a stressor can drive diversity in microbial strategies.

evolutionary biology↗

Epigenetic variation can promote adaptation by smoothing rugged fitness landscapes

Heritable non-genetic phenotypic variation--broadly, epigenetics--can potentially influence evolutionary outcomes as direct targets of selection or through interactions with genetic variation. While their evolutionary benefits in generating phenotypic diversity in changing environments is well-characterized, there has been relatively little consideration of how the joint influence of epigenetic changes and mutations would affect traversal of multi-peak adaptive landscapes. Here, we discover general principles for how epigenetics, by generating an epigenetic quasispecies (clusters of semi-stable phenotypes mapped to a single genotype), tends to improve adaptive outcomes of an asexual population on rugged fitness landscapes even without environmental change. In particular, rapid epigenetic changes can sometimes smooth out suboptimal fitness peaks through incorporating fitness contributions of epimutations, allowing access to better adaptive outcomes. Remarkably, the average impact of epigenetics is more strongly influenced by an approximate balance between switching rates rather than the absolute rate at which those switches occur. These findings demonstrate that epigenetic changes can be influential even without having strong heritability and have a striking, yet generally invisible, beneficial role in shaping a populations adaptive trajectory. Significance StatementSelection can act upon individuals with epigenetic differences, but it is unclear how much long-term effect this can have on evolutionary trajectories if the epigenetic changes only last a limited number of generations. When the environment changes or more than one functionality is needed simultaneously, it is apparent how bet hedging or division of labour can be advantageous, but what about in a single, constant environment? Here, we find that epigenetics, by allowing individuals rapid yet heritable access to multiple alternate phenotypes, can change the outcome of genetic evolution and has the tendency to remove local fitness peaks and allow adaptation to find higher optima. As such, epigenetics, despite being transient, can profoundly affect adaptive trajectories.

evolutionary biology↗

Adaptation strategies of iron-oxidizing bacteria Gallionella and Zetaproteobacteria crossing the marine-freshwater barrier

Iron-oxidizing Betaproteobacteria and Zetaproteobacteria are generally associated with freshwater and marine environments, respectively. Despite repeated cross-environment observations of these taxa, there has been no focused exploration of genomes of marine Gallionella (Betaproteobacteria) to understand transitions between freshwater and marine habitats. Consequently, their roles in these environments remain uncertain. Here, we present strong evidence for co-occurrence of Gallionella and Zetaproteobacteria at deep-sea hydrothermal vents at the Arctic Mid-Ocean Ridges through metagenomic analyses. Phylogenomics analysis of Gallionella metagenome-assembled genomes (MAGs) suggests that seawater adaptation is an evolutionary event which occurred multiple times in distinct lineages. Similarly, several distinct evolutionary events for freshwater and terrestrial Mariprofundus and other Zetaproteobacteria are predicted. The presence of cyc2 iron oxidation genes in co-occurring marine Betaproteobacteria and Zetaproteobacteria implies an overlap in niches of these iron-oxidizers. Functional enrichment analyses reveal genetic differences between marine MAGs of both iron-oxidizing groups and their terrestrial aquatic counterparts linked to salinity adaptation. Though scanning electron microscopy confirms the presence of Fe(III) oxyhydroxide stalks where Gallionella and Mariprofundus co-occur, Gallionella MAGs from hydrothermal vents lack evidence of putative stalk formation genes. Mariprofundus is therefore the likely sole stalk-producing iron-oxidizer in this environment. Conversely, discovery of putative stalk formation genes in Mariprofundus MAGs across the marine-freshwater barrier suggests that Fe(III) oxyhydroxide stalks might not be an exclusive signature for single iron-oxidizing taxa in marine and freshwater environments. Our research provides novel insights into the iron-oxidizing capacities, stalk production, environmental adaptation, and evolutionary transitions between marine and freshwater habitats for Gallionella and Zetaproteobacteria. ImportanceIron-oxidizing bacteria play an important role in the global cycling of iron, carbon, and other metals. While it has previously been assumed that bacterial evolution does not frequently involve crossing the salinity barrier, recent studies indicate that such occurrences are more common than previously thought. Our study offers strong evidence that this also happens among iron-oxidizing bacteria, with new insights into how these bacteria adapt to the new environment, including hydrothermal vents and freshwater habitats. In addition, we emphasize the importance of accurate iron-oxidizing taxa identification through sequencing, rather than relying solely on the morphology of Fe(III) oxyhydroxides and environment. On a larger scale, microorganisms within established communities needing to respond to changes in salinity due to events like seawater intrusion in coastal aquifers underscore the importance of knowledge of transitions across habitat types with different salt concentration.

microbiology↗

Novel hydrogen- and iron-oxidizing sheath-producing Zetaproteobacteria thrive at the Favne deep-sea hydrothermal vent field

Iron oxidizing Zetaproteobacteria are well-known to colonize deep-sea hydrothermal vent fields around the world where iron-rich fluids are discharged into oxic seawater. How inter-field and intra-field differences in geochemistry influence the diversity of Zetaproteobacteria, however, remains largely unknown. Here, we characterize Zetaproteobacteria phylogenomic diversity, metabolic potential, and morphologies of the iron oxides they form, with a focus on the recently discovered F[a]vne vent field. Located along the Mohns ridge in the Arctic, this vent field is a unique study site with vent fluids containing both iron and hydrogen with thick iron microbial mats (Fe mats) covering porously venting high-temperature (227-267 {degrees}C) black smoker chimneys. Through genome-resolved metagenomics and microscopy, we demonstrate that the Fe mats at F[a]vne are dominated by tubular iron oxide sheaths, likely produced by Zetaproteobacteria of genus Ghiorsea. With these structures, Ghiorsea may provide a surface area for members of other abundant taxa such as Campylobacterota, Gammaproteobacteria and Alphaproteobacteria. Furthermore, Ghiorsea likely oxidizes both iron and hydrogen present in the fluids, with several Ghiorsea populations co-existing in the same niche. Homologues of Zetaproteobacteria Ni,Fe hydrogenases and iron oxidation gene cyc2 were found in genomes of other community members, suggesting exchange of these genes could have happened in similar environments. Our study provides new insights into Zetaproteobacteria in hydrothermal vents, their diversity, energy metabolism and niche formation. ImportanceKnowledge on microbial iron oxidation is important for understanding the cycling of iron, carbon, nitrogen, nutrients, and metals. The current study yields important insights into the niche sharing, diversification, and Fe(III) oxyhydroxide morphology of Ghiorsea, an iron- and hydrogen oxidizing Zetaproteobacteria representative belonging to ZetaOTU9. The study proposes that Ghiorsea exhibits a more extensive morphology of Fe(III) oxyhydroxide than previously observed. Overall, the results increase our knowledge on potential drivers of Zetaproteobacteria diversity in iron microbial mats and can eventually be used to develop strategies for the cultivation of sheath-forming Zetaproteobacteria.

microbiology↗

Predicting experimental designs leading to rewiring of transcription program and evolution of anticipatory regulation in E. coli.

Environmental cues in an ecological niche are often temporal in nature. For instance, in temperate climates, temperature is higher in daytime compared to during night. In response to these temporal cues, bacteria have been known to exhibit anticipatory regulation, whereby they trigger response to a yet to appear cue, anticipating its actual arrival in the near future. Such an anticipatory response in known to enhance Darwinian fitness, and hence, is likely an important feature of regulatory networks in microorganisms. However, the conditions under which an anticipatory response evolves as an adaptive response are not known. In this work, we develop a quantitative model to study response of a population to two temporal environmental cues, and predict variables which are likely important for evolution of anticipatory regulatory response. We follow this with experimental evolution of E. coli in alternating environments of a pentose sugar, rhamnose, and an oxidative stress molecule, paraquat for more than 800 generations. We demonstrate that growth in this cyclical environment leads to evolution of anticipatory regulation, whereby, exposure to rhamnose leads to partial induction of the oxidative stress response regulon. As a result, pre-exposure to rhamnose leads to a greater fitness in paraquat environment. Overall, we show that in niches where environmental stimuli have a cyclical nature, anticipatory regulation can evolve as an adaptive strategy, in a time course of a few hundred generations. This contributes to our understanding of how environment shapes the topology of regulatory networks in an organism.

microbiology↗