Microbial colonization and controls in dryland systems

Drylands constitute the most extensive terrestrial biome, covering more than one-third of the Earth's continental surface. In these environments, stress limits animal and plant life, so life forms that can survive desiccation and then resume growth following subsequent wetting assume the foremost role in ecosystem processes. In this Review, we describe how these organisms assemble in unique soil- and rock-surface communities to form a thin veneer of mostly microbial biomass across hot and cold deserts. These communities mediate inputs and outputs of gases, nutrients and water from desert surfaces, as well as regulating weathering, soil stability, and hydrological and nutrient cycles. The magnitude of regional and global desert-related environmental impacts is affected by these surface communities; here, we also discuss the challenges for incorporating the consideration of these communities and their effects into the management of dryland resources.     

Phylogenetic diversity of stress signalling pathways in fungi

Background  

Microbes must sense environmental stresses, transduce these signals and mount protective responses to survive in hostile environments. In this study we have tested the hypothesis that fungal stress signalling pathways have evolved rapidly in a niche-specific fashion that is independent of phylogeny. To test this hypothesis we have compared the conservation of stress signalling molecules in diverse fungal species with their stress resistance. These fungi, which include ascomycetes, basidiomycetes and microsporidia, occupy highly divergent niches from saline environments to plant or mammalian hosts.     

Protozoan Cysts Act as a Survival Niche and Protective Shelter for Foodborne Pathogenic Bacteria

The production of cysts, an integral part of the life cycle of many free-living protozoa, allows these organisms to survive adverse environmental conditions. Given the prevalence of free-living protozoa in food-related environments, it is hypothesized that these organisms play an important yet currently underinvestigated role in the epidemiology of foodborne pathogenic bacteria. Intracystic bacterial survival is highly relevant, as this would allow bacteria to survive the stringent cleaning and disinfection measures applied in food-related environments. The present study shows that strains of widespread and important foodborne bacteria (Salmonella enterica, Escherichia coli, Yersinia enterocolitica, and Listeria monocytogenes) survive inside cysts of the ubiquitous amoeba Acanthamoeba castellanii, even when exposed to either antibiotic treatment (100 μg/ml gentamicin) or highly acidic conditions (pH 0.2) and resume active growth in broth media following excystment. Strain- and species-specific differences in survival periods were observed, with Salmonella enterica surviving up to 3 weeks inside amoebal cysts. Up to 53% of the cysts were infected with pathogenic bacteria, which were located in the cyst cytosol. Our study suggests that the role of free-living protozoa and especially their cysts in the persistence and epidemiology of foodborne bacterial pathogens in food-related environments may be much more important than hitherto assumed.     

Incorporation of Exogenous Fatty Acids Protects Enterococcus faecalis from Membrane-Damaging Agents

Enterococcus faecalis is a commensal bacterium of the mammalian intestine that can persist in soil and aquatic systems and can be a nosocomial pathogen to humans. It employs multiple stress adaptation strategies in order to survive such a wide range of environments. Within this study, we sought to elucidate whether membrane fatty acid composition changes are an important component for stress adaptation. We noted that E. faecalis OG1RF was capable of changing its membrane composition depending upon growth phase and temperature. The organism also readily incorporated fatty acids from bile, serum, and medium supplemented with individual fatty acids, often dramatically changing the membrane composition such that a single fatty acid was predominant. Growth in either low levels of bile or specific individual fatty acids was found to protect the organism from membrane challenges such as high bile exposure. In particular, we observed that when grown in low levels of bile, serum, or the host-derived fatty acids oleic acid and linoleic acid, E. faecalis was better able to survive the antibiotic daptomycin. Interestingly, the degree of membrane saturation did not appear to be important for protection from the stressors examined here; instead, it appears that a specific fatty acid or combination of fatty acids is critical for stress resistance.     

Wastewater as a fertility source for novel bacteriophages against multi-drug resistant bacteria

Antibiotic resistance is a common and serious public health worldwide. As an alternative to antibiotics, bacteriophage (phage) therapy offers one of the best solutions to antibiotic resistance. Bacteriophages survive where their bacterial hosts are found; thus, they exist in almost all environments and their applications are quite varied in the medical, environmental, and industrial fields. Moreover, a single phage or a mixture of phages can be used in phage therapy; mixed phages tend to be more effective in reducing the number and/or activity of pathogenic bacteria than that of a single phage.     

Perception and Regulatory Principles of Microbial Growth Control

Fast growth represents an effective strategy for microbial organisms to survive in competitive environments. To accomplish this task, cells must adapt their metabolism to changing nutrient conditions in a way that maximizes their growth rate. However, the regulation of the growth related metabolic pathways can be fundamentally different among microbes. We therefore asked whether growth control by perception of the cell’s intracellular metabolic state can give rise to higher growth than by direct perception of extracellular nutrient availability. To answer this question, we created a simplified dynamical computer model of a cellular metabolic network whose regulation was inferred by an optimization approach. We used this model for a competing species experiment, where a species with extracellular nutrient perception competes against one with intracellular nutrient perception by evaluating their respective average growth rate. We found that the intracellular perception is advantageous under situations where the up and down regulation of pathways cannot follow the fast changing nutrient availability in the environment. In this case, optimal regulation ignores any other nutrients except the most preferential ones, in agreement with the phenomenon of catabolite repression in prokaryotes. The corresponding metabolic pathways remain activated, despite environmental fluctuations. Therefore, the cell can take up preferential nutrients as soon as they are available without any prior regulation. As a result species that rely on intracellular perception gain a relevant fitness advantage in fluctuating nutrient environments, which enables survival by outgrowing competitors.     

Bacterial persistence: a model of survival in changing environments

The persistence phenotype is an epigenetic trait exhibited by a subpopulation of bacteria, characterized by slow growth coupled with an ability to survive antibiotic treatment. The phenotype is acquired via a spontaneous, reversible switch between normal and persister cells. These observations suggest that clonal bacterial populations may use persister cells, whose slow division rate under growth conditions leads to lower population fitness, as an "insurance policy" against antibiotic encounters. We present a model of Escherichia coli persistence, and using experimentally derived parameters for both wild type and a mutant strain (hipQ) with markedly different switching rates, we show how fitness loss due to slow persister growth pays off as a risk-reducing strategy. We demonstrate that wild-type persistence is suited for environments in which antibiotic stress is a rare event. The optimal rate of switching between normal and persister cells is found to depend strongly on the frequency of environmental changes and only weakly on the selective pressures of any given environment. In contrast to typical examples of adaptations to features of a single environment, persistence appears to constitute an adaptation that is tuned to the distribution of environmental change.     

Regional zooplankton biodiversity provides limited buffering of pond ecosystems against climate change

1. Climate change and other human-driven environmental perturbations are causing reductions in biodiversity and impacting the functioning of ecosystems on a global scale. Metacommunity theory suggests that ecosystem connectivity may reduce the magnitude of these impacts if the regional species pool contains functionally redundant species that differ in their environmental tolerances. Dispersal may increase the resistance of local ecosystems to environmental stress by providing regional species with traits adapted to novel conditions. 2. We tested this theory by subjecting freshwater zooplankton communities in mesocosms that were either connected to or isolated from the larger regional species pool to a factorial manipulation of experimental warming and increased salinity. 3. Compensation by regional taxa depended on the source of stress. Warming tolerant regional taxa partially compensated for reductions in heat sensitive local taxa but similar compensation did not occur under increased salinity. 4. Dispersal-mediated species invasions dampened the effects of warming on summer net ecosystem productivity. However, this buffering effect did not occur in the fall or for periphyton growth, the only other ecosystem function affected by the stress treatments. 5. The results indicate that regional biodiversity can provide insurance in a dynamic environment but that the buffering capacity is limited to some ecosystem processes and sources of stress. Maintaining regional biodiversity and habitat connectivity may therefore provide some limited insurance for local ecosystems in changing environments, but is unable to impart resistance against all sources of environmental stress.     

Bacillus subtilis: A plant-growth promoting rhizobacterium that also impacts biotic stress

Plants encounter many biotic agents, such as viruses, bacteria, nematodes, weeds, and arachnids. These entities induce biotic stress in their hosts by disrupting normal metabolism, and as a result, limit plant growth and/or are the cause of plant mortality. Some biotic agents, however, interact symbiotically or synergistically with their host plants. Some microbes can be beneficial to plants and perform the same role as chemical fertilizers and pesticides, acting as a biofertilizer and/or biopesticide. Plant growth promoting rhizobacteria (PGPR) can significantly enhance plant growth and represent a mutually helpful plant-microbe interaction. Bacillus species are a major type of rhizobacteria that can form spores that can survive in the soil for long period of time under harsh environmental conditions. Plant growth is enhanced by PGPR through the induction of systemic resistance, antibiosis, and competitive omission. Thus, the application of microbes can be used to induce systemic resistance in plants against biotic agents and enhance environmental stress tolerance. Bacillus subtilis exhibits both a direct and indirect biocontrol mechanism to suppress disease caused by pathogens. The direct mechanism includes the synthesis of many secondary metabolites, hormones, cell-wall-degrading enzymes, and antioxidants that assist the plant in its defense against pathogen attack. The indirect mechanism includes the stimulation of plant growth and the induction of acquired systemic resistance. Bacillus subtilis can also solubilize soil P, enhance nitrogen fixation, and produce siderophores that promote its growth and suppresses the growth of pathogens. Bacillus subtilis enhances stress tolerance in their plant hosts by inducing the expression of stress-response genes, phytohormones, and stress-related metabolites. The present review discusses the activity of B. subtilis in the rhizosphere, its role as a root colonizer, its biocontrol potential, the associated mechanisms of biocontrol and the ability of B. subtilis to increase crop productivity under conditions of biotic and abiotic stress.     

Distinct cold tolerance traits independently vary across genotypes in Drosophila melanogaster

Cold tolerance, the ability to cope with low temperature stress, is a critical adaptation in thermally variable environments. An individual's cold tolerance comprises several traits including minimum temperatures for growth and activity, ability to survive severe cold, and ability to resume normal function after cold subsides. Across species, these traits are correlated, suggesting they were shaped by shared evolutionary processes or possibly share physiological mechanisms. However, the extent to which cold tolerance traits and their associated mechanisms covary within populations has not been assessed. We measured five cold tolerance traits—critical thermal minimum, chill coma recovery, short- and long-term cold tolerance, and cold-induced changes in locomotor behavior—along with cold-induced expression of two genes with possible roles in cold tolerance (heat shock protein 70 and frost)—across 12 lines of Drosophila melanogaster derived from a single population. We observed significant genetic variation in all traits, but few were correlated across genotypes, and these correlations were sex-specific. Further, cold-induced gene expression varied by genotype, but there was no evidence supporting our hypothesis that cold-hardy lines would have either higher baseline expression or induction of stress genes. These results suggest cold tolerance traits possess unique mechanisms and have the capacity to evolve independently.     

Drought exposure leads to rapid acquisition and inheritance of herbicide resistance in the weed Alopecurus myosuroides

Globally, herbicide resistance in weeds poses a threat to food security. Resistance evolves rapidly through the co‐option of a suite of physiological mechanisms that evolved to allow plants to survive environmental stress. Consequently, we hypothesize that stress tolerance and herbicide resistance are functionally linked. We address two questions: (i) does exposure to stress in a parental generation promote the evolution of resistance in the offspring? (ii) Is such evolution mediated through non‐genetic mechanisms? We exposed individuals of a grass weed to drought, and tested whether this resulted in herbicide resistance in the first generation. In terms of both survival and dry mass, we find enhanced resistance to herbicide in the offspring of parents that had been exposed to drought. Our results suggest that exposure of weeds to drought can confer herbicide resistance in subsequent generations, and that the mechanism conferring heritability of herbicide resistance is non‐genetic.     

Pathogen exposure reduces sexual dimorphism in a host’s upper thermal limits

The climate is warming at an unprecedented rate, pushing many species toward and beyond the upper temperatures at which they can survive. Global change is also leading to dramatic shifts in the distribution of pathogens. As a result, upper thermal limits and susceptibility to infection should be key determinants of whether populations continue to persist, or instead go extinct. Within a population, however, individuals vary in both their resistance to both heat stress and infection, and their contributions to vital growth rates. No more so is this true than for males and females. Each sex often varies in their response to pathogen exposure, thermal tolerances, and particularly their influence on population growth, owing to the higher parental investment that females typically make in their offspring. To date, the interplay between host sex, infection, and upper thermal limits has been neglected. Here, we explore the response of male and female Daphnia to bacterial infection and static heat stress. We find that female Daphnia, when uninfected, are much more resistant to static heat stress than males, but that infection negates any advantage that females are afforded. We discuss how the capacity of a population to cope with multiple stressors may be underestimated unless both sexes are considered simultaneously.     

Low-temperature sensors in bacteria

Bacteria are ubiquitous colonizers of various environments and host organisms, and they are therefore often subjected to drastic temperature alterations. Temperature alterations set demands on these colonizers, in that the bacteria need to readjust their biochemical constitution and physiology in order to survive and resume growth at the new temperature. Furthermore, temperature alteration is also a main factor determining the expression or repression of bacterial virulence functions. To cope with temperature variation, bacteria have devices for sensing temperature alterations and a means of translating this sensory event into a pragmatic gene response. While such regulatory cascades may ultimately be complicated, it appears that they contain primary sensor machinery at the top of the cascade. The functional core of such machinery is usually that of a temperature-induced conformational or physico-chemical change in the central constituents of the cell. In a sense, a bacterium can use structural alterations in its biomolecules as the primary thermometers or thermostats.     

Persistence and resistance as complementary bacterial adaptations to antibiotics

Bacterial persistence represents a simple of phenotypic heterogeneity, whereby a proportion of cells in an isogenic bacterial population can survive exposure to lethal stresses such as antibiotics. In contrast, genetically based antibiotic resistance allows for continued growth in the presence of antibiotics. It is unclear, however, whether resistance and persistence are complementary or alternative evolutionary adaptations to antibiotics. Here, we investigate the co‐evolution of resistance and persistence across the genus Pseudomonas using comparative methods that correct for phylogenetic nonindependence. We find that strains of Pseudomonas vary extensively in both their intrinsic resistance to antibiotics (ciprofloxacin and rifampicin) and persistence following exposure to these antibiotics. Crucially, we find that persistence correlates positively to antibiotic resistance across strains. However, we find that different genes control resistance and persistence implying that they are independent traits. Specifically, we find that the number of type II toxin–antitoxin systems (TAs) in the genome of a strain is correlated to persistence, but not resistance. Our study shows that persistence and antibiotic resistance are complementary, but independent, evolutionary adaptations to stress and it highlights the key role played by TAs in the evolution of persistence.     

Stress-induced assortative mating and the evolution of stress resistance

We show with a model that variation in environmental stress between generations facilitates the evolution of stress resistance through assortative mating. Stress induces delayed maturation of susceptible phenotypes, segregating their fertile period from resistant phenotypes. Assortment of mates enhances the responsiveness of populations to natural selection by inflating genetic variance. Thus, positive selection and inflated genetic variance in stressful environments can cause a strong evolutionary increase in resistance. By contrast, benign environments do not segregate phenotypes, and the random mating among phenotypes deflates genetic variance, leading to a weaker response to selection against resistance, assuming that resistance is costly. When environments vary randomly from benign to stressful, populations respond asymmetrically to negative and positive selection. This asymmetry (1) accelerates fixation of a resistance allele if resistance is generally favoured (stressful generations more frequent) but delays the loss of the allele if it is generally disfavoured (benign generations more frequent), and (2) it can push a resistance allele to fixation even when long‐term costs modestly exceed benefits. When resistance alleles pleiotropically delay mating, stress‐induced random mating has complementary effects. Serial autocorrelation in the stressor amplifies these effects. These results suggest a novel mechanism for the persistence of resistance polymorphisms.