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bioRxiv2016

A Critical, Nonlinear Threshold Dictates Bacterial Invasion and Initial Kinetics During Influenza

Secondary bacterial infections increase morbidity and mortality of influenza A virus (IAV) infections. Bacteria are able to invade due to virus-induced depletion of alveolar macrophages (AMs), but this is not the only contributing factor. By analyzing a kinetic model, we uncovered a nonlinear initial dose threshold that is dependent on the amount of virus-induced AM depletion. The threshold separates the growth and clearance phenotypes such that bacteria decline for dose-AM depletion combinations below the threshold, stay constant near the threshold, and increase above the threshold. In addition, the distance from the threshold correlates to the growth rate. Because AM depletion changes throughout an IAV infection, the dose requirement for bacterial invasion also changes accordingly. Using the threshold, we found that the dose requirement drops dramatically during the first 7d of IAV infection. We then validated these analytical predictions by infecting mice with doses below or above the predicted threshold over the course of IAV infection. These results identify the nonlinear way in which two independent factors work together to support successful post-influenza bacterial invasion. They provide insight into coinfection timing, the heterogeneity in outcome, the probability of acquiring a coinfection, and the use of new therapeutic strategies to combat viral-bacterial coinfections.

Microbiology↗

bioRxiv2016

A Zika virus-associated microcephaly case with background exposure to STORCH agents

We present a case of microcephaly associated with Zika virus (ZIKV) in a chronological, multimodal imaging approach, illustrating the hallmarks of this disease on intrauterine morphological ultrasound, transfontanelar ultrasound, computed tomography (CT) and magnetic resonance imaging (MRI). We also determined the serological e immunological status of the mother and newborn. Noticeably, there was evidence for maternal infection by ZIKV, cytomegalovirus (CMV), herpes simplex virus (HSV), dengue virus (DENV) and Toxoplasma gondii, which indicates a possible role of previous exposures to STORCH agents and possibly comorbidities in the severe fetal congenital manifestation.\n\nAuthor SummaryZika virus (ZIKV) is an emerging mosquito-borne arbovirus causing dengue-like symptoms. In humans the illness is characterized by malaise and cutaneous rash and absent or short-termed fever. Recently, the Brazilian Ministry of Health reported an outbreak of microcephaly in Brazil as a delayed effect of the 2014-2015 outbreak of ZIKV in the Northeast of Brazil. A 20-fold increase in the notifications of newborns with microcephaly was documented during the second semester of 2015. This increase was almost immediately found to be associated with ZIKV infections, both in Brazil and, retrospectively, in French Polynesia. Herein we report a case of microcephaly associated with ZIKV and we also present evidence of other maternal infections. Our results indicated that, both mother and microcephaly infant had immunologic status compatible with previous exposure (in the mother) by STORCH agents. These indicate a possible role of previous exposures and possibly comorbidities in the severe fetal congenital manifestation. {square}

Microbiology↗

bioRxiv2016

Bacteria regulate choanoflagellate development with lipid activators, inhibitors, and synergists

In choanoflagellates, the closest living relatives of animals, multicellular \"rosette\" development is regulated by environmental bacteria. The simplicity of this evolutionarily-relevant interaction provides an opportunity to identify the molecules and regulatory logic underpinning bacterial regulation of development. We find that the rosette-inducing bacterium Algoriphagus machipongonensis produces three structurally divergent classes of bioactive lipids that, together, activate, enhance, and inhibit rosette development in the choanoflagellate S. rosetta. One class of molecules, the lysophosphatidylethanolamines (LPEs), elicits no response on its own, but synergizes with activating sulfonolipid rosette inducing factors (RIFs) to recapitulate the full bioactivity of live Algoriphagus. LPEs, while ubiquitous in bacteria and eukaryotes, have not previously been implicated in the regulation of a host-microbe interaction. This study reveals that multiple bacterially-produced lipids converge to activate, enhance, and inhibit multicellular development in a choanoflagellate.\n\nSignificance StatementBacterial symbionts profoundly influence the biology of their animal hosts, yet complex interactions between animals and their resident bacteria often make it challenging to characterize the molecules and mechanisms. Simple model systems can reveal fundamental processes underlying interactions between eukaryotes and their associated microbial communities, and provide insight into how bacteria regulate animal biology. In this study we isolate and characterize bacterial molecules that regulate multicellular development in the closest living relatives of animals, the choanoflagellate. We find that multiple bacterially-derived lipids converge to activate, enhance, and inhibit choanoflagellate multicellular development.

Microbiology↗

bioRxiv2016

Self-driven jamming in growing microbial populations

In natural settings, microbes tend to grow in dense populations [1-4] where they need to push against their surroundings to accommodate space for new cells. The associated contact forces play a critical role in a variety of population-level processes, including biofilm formation [5-7], the colonization of porous media [8, 9], and the invasion of biological tissues [10-12]. Although mechanical forces have been characterized at the single cell level [13-16], it remains elusive how collective pushing forces result from the combination of single cell forces. Here, we reveal a collective mechanism of confinement, which we call self-driven jamming, that promotes the build-up of large mechanical pressures in microbial populations. Microfluidic experiments on budding yeast populations in space-limited environments show that self-driven jamming arises from the gradual formation and sudden collapse of force chains driven by microbial proliferation, extending the framework of driven granular matter [17-20]. The resulting contact pressures can become large enough to slow down cell growth by delaying the cell cycle in the G1 phase and to strain or even destroy the microenvironment through crack propagation. Our results suggest that self-driven jamming and build-up of large mechanical pressures is a natural tendency of microbes growing in confined spaces, contributing to microbial pathogenesis and biofouling [21-26].

Microbiology↗

bioRxiv2016

Host Gut Motility and Bacterial Competition Drive Instability in a Model Intestinal Microbiota

The gut microbiota is a complex consortium of microorganisms with the ability to influence important aspects of host health and development. Harnessing this microbial organ for biomedical applications requires clarifying the degree to which host and bacterial factors act alone or in combination to govern the stability of specific lineages. To address this we combined bacteriological manipulation and light sheet fluorescence microscopy to monitor the dynamics of a defined two-species microbiota within the vertebrate gut. We observed that the interplay between each population and the gut environment produced distinct spatiotemporal patterns. Consequently, one species dominates while the other experiences dramatic collapses that are well fit by a stochastic mathematical model. Modeling revealed that bacterial competition could only partially explain the observed phenomena, suggesting that a host factor is also important in shaping the community. We hypothesized the host determinant to be gut motility, and tested this mechanism by measuring colonization in hosts with enteric nervous system dysfunction due to mutation in the Hirschsprung disease locus ret. In mutant hosts we found reduced gut motility and, confirming our hypothesis, robust coexistence of both bacterial species. This study provides evidence that host-mediated spatial structuring and stochastic perturbation of communities along with bacterial competition drives population dynamics within the gut. In addition, this work highlights the capacity of the enteric nervous system to affect stability of gut microbiota constituents, demonstrating that the gut-brain axis is bidirectional. Ultimately, these findings will help inform disease mitigation strategies focused on engineering the intestinal ecosystem.

Microbiology↗

bioRxiv2016

Antibiotic Stress Selects against Cooperation in a Pathogenic Bacterium

Ecological antagonisms such as predation, parasitism, competition, and abiotic environmental stress play key roles in shaping population biology, in particular by inducing stress responses and selecting for tolerant or resistant phenotypes. Little is known, however, about their impact on social traits, such as the production of public goods. Evolutionary trade-off theory predicts that adaptation to stresses should lessen investments in costly helping behaviours when cooperation does not increase resistance or tolerance, but support for this prediction is scarce. We employed theory and experiments to investigate how ecological antagonism influences social dynamics and resistance evolution in the pathogenic bacterium Pseudomonas aeruginosa. We subjected two clones of bacterium to four doses of antibiotics and assessed growth and frequencies of public goods producing and non-producing genotypes. Our results show that abiotic stress selects against public goods production. Specifically, we found that non-producers of costly iron chelating molecules (siderophores) most rapidly increased in frequency under intermediate antibiotic pressure. Moreover, the dominance of non-producers in mixed cultures was associated with higher survival and resistance to antibiotics than in either producer or non-producer monocultures. Mathematical modelling explains this counterintuitive result, and shows how these qualitative patterns are predicted to generalise to many other systems. Our results shed light on the complex interactions between social traits and ecological antagonisms, and in particular the consequences for bacterial social evolution and antibiotic resistance.

Microbiology↗

bioRxiv2016

Stable host gene expression in the gut of adult Drosophila melanogaster with different bacterial mono-associations

There is growing evidence that the microbes found in the digestive tracts of animals influence host biology, but we still do not understand how this comes about. Here, we evaluated how different microbial species commonly associated with laboratory-reared Drosophila melanogaster impact host biology at the level of gene expression in the dissected adult gut or the entire adult organism. We observed that guts from gnotobiotic animals associated from the embryonic stage with either zero, one or three bacterial species demonstrated indistinguishable transcriptional profiles. Additionally, we found that the gut transcriptional profiles of animals reared in the presence of the yeast Saccharomyces cerevisiae alone or in combination with bacteria could recapitulate those of conventionally-reared animals. In contrast, we found whole body transcriptional profiles of conventionally-reared animals were distinct from all of the gnotobiotic treatments tested. Our data suggest that adult flies are insensitive to the ingestion of different bacterial species but that prior to adulthood, different microbes impact the host in ways that lead to global transcriptional differences observable across the whole adult body.

Microbiology↗

bioRxiv2016

Acute induction of anomalous blood clotting by molecular amplification of highly substoichiometric levels of bacterial lipopolysaccharide (LPS)

It is well known that a variety of inflammatory diseases are accompanied by hypercoagulability, and a number of more-or-less longer-term signalling pathways have been shown to be involved. In recent work, we have suggested a direct and primary role for bacterial lipopolysaccharide in this hypercoagulability, but it seems never to have been tested directly. Here we show that the addition of tiny concentrations (0.2 ng.L-1) of bacterial lipopolysaccharide (LPS) to both whole blood and platelet-poor plasma of normal, healthy donors leads to marked changes in the nature of the fibrin fibres so formed, as observed by ultrastructural and fluorescence microscopy (the latter implying that the fibrin is actually in an amyloid {beta}-sheet-rich form. They resemble those seen in a number of inflammatory (and also amyloid) diseases, consistent with an involvement of LPS in their aetiology. These changes are mirrored by changes in their viscoelastic properties as measured by thromboelastography. Since the terminal stages of coagulation involve the polymerisation of fibrinogen into fibrin fibres, we tested whether LPS would bind to fibrinogen directly. We demonstrated this using isothermal calorimetry. Finally, we show that these changes in fibre structure are mirrored when the experiment is done simply with purified fibrinogen and thrombin ({+/-} 0.2 ng.L-1 LPS). This ratio of concentrations of LPS:fibrinogen in vivo represents a molecular amplification by the LPS of more than 108-fold, a number that is probably unparalleled in biology. The observation of a direct effect of such highly substoichiometric amounts of LPS on both fibrinogen and coagulation can account for the role of very small numbers of dormant bacteria in disease progression, and opens up this process to further mechanistic analysis and possible treatment.\n\nSignificance statementMost chronic diseases (including those classified as cardiovascular, neurodegenerative, or autoimmune) are accompanied by long-term inflammation. Although typically mediated by inflammatory cytokines, the origin of this inflammation is unclear. We have suggested that one explanation is a dormant microbiome that can shed the highly inflammatory lipopolysaccharide LPS. Such inflammatory diseases are also accompanied by a hypercoagulable phenotype. We here show directly (using 6 different methods) that very low concentrations of LPS can affect the terminal stages of the coagulation properties of blood and plasma significantly, and that this may be mediated via a direct binding of LPS to a small fraction of fibrinogen monomers as assessed biophysically. Such amplification methods may be of more general significance.

Microbiology↗

bioRxiv2016

Increasing tolerance of hospital Enterococcus faecium to hand-rub alcohols

Alcohol-based hand rubs are international pillars of hospital infection control, restricting transmission of pathogens such as Staphylococcus aureus. Despite this success, health care infections caused by Enterococcus faecium (Efm) - another multidrug resistant pathogen - are increasing. We tested alcohol tolerance of 139 hospital Efm isolates, obtained between 1997 and 2015 and found Efm post-2010 were 10-fold more tolerant to alcohol killing than older isolates. Using a mouse infection control model, we then showed that alcohol tolerant Efm resisted standard 70% isopropanol surface disinfection and led to gastrointestinal colonization significantly more often than alcohol sensitive Efm. We next looked for bacterial genomic signatures of adaptation. Tolerant Efm have independently accumulated mutations modifying genes involved in carbohydrate uptake and metabolism. Mutagenesis confirmed their roles in isopropanol tolerance. These findings suggest bacterial adaptation and complicate infection control recommendations. Additional policies and procedures to prevent Efm spread are required.

Microbiology↗

bioRxiv2016

Dynamic substrate preferences and predicted metabolic properties of a simple microbial consortium

Microorganisms are typically found as complex microbial communities that altogether govern global biogeochemical cycles. Microbes have developed highly regulated metabolic capabilities to efficiently use available substrates including preferential substrate usage that can result in diauxic shifts. This and other metabolic behaviors have been discovered in studies of microbes in monoculture when grown on low-complexity (e.g. two-component) mixtures of substrates, however, little is known about how species partition environmental substrates through substrate competition in more complex substrate mixtures. Here we use exometabolomic profiling to examine the time-varying substrate depletion from a mixture of 19 amino acids and glucose by two Pseudomonads and one Bacillus species isolated from ground water. We examine if the first substrates depleted result in maximal growth rate, or relate to growth medium or biomass composition and find surprisingly few correlations. Patterns of substrate depletion are modeled, and these models are used to examine if substrate usage preferences and substrate depletion kinetics of three microbial isolates can be used to predict the metabolism of the pooled isolates in co-culture. We find that most of the substrates fit the model predictions, indicating that the microbes are not altering their behaviors for these substrates in the presence of competitors. Glucose and histidine were depleted more slowly than predicted, while proline, glycine, glutamate, lysine, and arginine were all consumed significantly faster; these compounds highlight substrates that could be involved in species-species interactions within the consortium.\n\nAuthor ContributionsOE, TRN conceived and designed the experiments\n\nOE, BPB, SMK, SJ, RL performed the experiments\n\nOE, BPB, SJ, TRN analyzed the data\n\nOE, TRN wrote the manuscript\n\nTRN contributed materials and analysis tools

Microbiology↗

bioRxiv2016

Environmental modification via a quorum sensing molecule influences the social landscape of siderophore production

Bacteria produce a wide variety of exoproducts that favourably modify their environment and increase their fitness. These are often termed public goods because they are costly for individuals to produce and can be exploited by non-producers ( cheats). The outcome of conflict over public goods is dependent upon the prevailing environment and the phenotype of the individuals in competition. Many bacterial species use quorum sensing (QS) signalling molecules to regulate the production of public goods. QS therefore determines the cooperative phenotype of individuals, and influences conflict over public goods. In addition to their regulatory functions, many QS molecules have additional properties that directly modify the prevailing environment. This leads to the possibility that QS molecules could influence conflict over public goods indirectly through non-signalling effects, and the impact of this on social competition has not previously been explored. The Pseudomonas aeruginosa QS signal molecule PQS is a powerful chelator of iron which can cause an iron starvation response. Here we show that PQS stimulates a concentration-dependent increase in the cooperative production of iron scavenging siderophores, resulting in an increase in the relative fitness of non-producing siderophore cheats. This is likely due to an increased cost of siderophore output by producing cells and a concurrent increase in the shared benefits, which accrue to both producers and cheats. Although PQS can be a beneficial signalling molecule for P.aeruginosa, our data suggests that it can also render a siderophore-producing population vulnerable to competition from cheating strains. More generally our results indicate that the production of one social trait can indirectly affect the costs and benefits of another social trait.

Microbiology↗

bioRxiv2016

Genome reduction in an abundant and ubiquitous soil bacterial lineage

Although bacteria within the Verrucomicrobia phylum are pervasive in soils around the world, they are underrepresented in both isolate collections and genomic databases. Here we describe a single verrucomicrobial phylotype within the class Spartobacteria that is not closely related to any previously described taxa. We examined >1000 soils and found this spartobacterial phylotype to be ubiquitous and consistently one of the most abundant soil bacterial phylotypes, particularly in grasslands, where it was typically the most abundant phylotype. We reconstructed a nearly complete genome of this phylotype from a soil metagenome for which we propose the provisional name Candidatus Udaeobacter copiosus. The Ca. U. copiosus genome is unusually small for soil bacteria, estimated to be only 2.81 Mbp compared to the predicted effective mean genome size of 4.74 Mbp for soil bacteria. Metabolic reconstruction suggests that Ca. U. copiosus is an aerobic chemoorganoheterotroph with numerous amino acid and vitamin auxotrophies. The large population size, relatively small genome and multiple putative auxotrophies characteristic of Ca. U. copiosus suggests that it may be undergoing streamlining selection to minimize cellular architecture, a phenomenon previously thought to be restricted to aquatic bacteria. Although many soil bacteria need relatively large, complex genomes to be successful in soil, Ca. U. copiosus appears to have identified an alternate strategy, sacrificing metabolic versatility for efficiency to become dominant in the soil environment.

Microbiology↗

bioRxiv2016

Establishment and stability of the latent HIV-1 DNA reservoir

HIV-1 infection currently cannot be cured because the virus persists as integrated proviral DNA in long-lived cells despite years of suppressive antiretroviral therapy (ART). To characterize establishment, turnover, and evolution of viral DNA reservoirs we deep-sequenced the p17gag region of the HIV-1 genome from samples obtained after 3-18 years of suppressive ART from 10 patients. For each of these patients, whole genome deep-sequencing data of HIV-1 RNA populations before onset of ART were available from 6-12 longitudinal plasma samples spanning 5-8 years of untreated infection. This enabled a detailed analysis of the dynamics and origin of proviral DNA during ART. A median of 14% (range 0-42%) of the p17gag DNA sequences were overtly defective due to G-to-A hypermutation. The remaining sequences were remarkably similar to previously observed RNA sequences and showed no evidence of evolution over many years of suppressive ART. Most sequences from the DNA reservoirs were very similar to viruses actively replicating in plasma (RNA sequences) shortly before start of ART. The results do not support persistent HIV-1 replication as a mechanism to maintain the HIV-1 reservoir during suppressive therapy. Rather, the data indicate that viral DNA variants are turning over as long as patients are untreated and that suppressive ART halts this turnover.

Microbiology↗

bioRxiv2016

Evidence for reassortment of highly divergent novel rotaviruses from bats in Cameroon, without evidence for human interspecies transmissions

Bats are an important reservoir for pathogenic human respiratory and hemorrhagic viruses but only little is known about bat viruses causing gastroenteritis in humans, including rotavirus A strains (RVA). Only three RVA strains have been reported in bats in Kenya (straw-colored fruit bat) and in China (lesser horseshoe and a stoliczkas trident bat), being highly divergent from each other. To further elucidate the potential of bat RVAs to cause gastroenteritis in humans we started by investigating the genetic diversity of RVAs in fecal samples from 87 straw-colored fruit bats living in close contact with humans in Cameroon using metagenomics. Five samples contained significant numbers of RVA Illumina reads, sufficient to obtain their (near) complete genomes. A single RVA strain showed a close phylogenetic relationship with the Kenyan bat RVA strain in six gene segments, including VP7 (G25), whereas the other gene segments represented novel genotypes as ratified by the RCWG. The 4 other RVA strains were highly divergent from known strains (but very similar among each other) possessing all novel genotypes. Only the VP7 and VP4 genes showed a significant variability representing multiple novel G and P genotypes, indicating the frequent occurrence of reassortment events.\n\nComparing these bat RVA strains with currently used human RVA screening primers indicated that several of the novel VP7 and VP4 segments would not be detected in routine epidemiological screening studies. Therefore, novel VP6 based screening primers matching both human and bat RVAs were developed and used to screen samples from 25 infants with gastroenteritis living in close proximity with the studied bat population. Although RVA infections were identified in 36% of the infants, Sanger sequencing did not indicate evidence of interspecies transmissions.\n\nThis study identified multiple novel bat RVA strains, but further epidemiological studies in humans will have to assess if these viruses have the potential to cause gastroenteritis in humans.

Microbiology↗

bioRxiv2016

Monomorphic genotypes within a generalist lineage of Campylobacter jejuni show signs of global dispersion

The decreased costs of genome sequencing have increased capability to apply whole-genome sequence on epidemiological surveillance of zoonotic Campylobacter jejuni. However, knowledge about how genetically similar epidemiologically linked isolates can be is vital for correct application of this methodology. To address this issue in C. jejuni we investigated the spatial and temporal signals in the genomes of a major clonal complex and generalist lineage, ST-45 CC, by exploiting the population structure and genealogy and applying genome-wide association analysis of 340 isolates from across Europe collected over a wide time-range. The occurrence and strength of the geographical signal varied between sublineages and followed the clonal frame when present, while no evidence of a temporal signal was found. Certain sublineages of ST-45 CC formed discrete and genetically isolated clades to which geography and time had left only negligible traces in the genomes. We hypothesize that these ST-45 CC clades form globally expanded monomorphic clones possibly spread across Europe by migratory birds. In addition, we observed an incongruence between the genealogy of the strains and MLST typing, thereby challenging the existing clonal complex definition and use of a common MLST-based nomenclature for the ST-45 CC of C. jejuni.

Microbiology↗

bioRxiv2016

Potential pitfalls of FISH microscopy as assessment method for anaerobic digesters

In the present work we investigated how the state of a biogas reactor impacts the enumeration of prokaryotic cells by fluorescence in situ hybridisation (FISH). Therefore, the correlation between gas production and FISH hybridisation rates was analysed in different anaerobic digester sludges. High gasification activity coincided with high hybridisation rates. Low hybridisation rates were especially achieved with reactor samples subjected to long starvation periods showing low biogas production.\n\nBased on our findings we conclude that samples for FISH analysis should be fixed as soon as possible to prevent a loss of microbial activity resulting in lower FISH signals. Furthermore, the location of sampling is of importance, since samples from different fermenters within the same biogas plant also varied strongly in their FISH hybridisation rate. Our results indicate that FISH could be a useful method for assessing the metabolic state of microorganisms in anaerobic digester plants.

Microbiology↗

bioRxiv2016

Metagenomic covariation along densely sampled environmental gradients in the Red Sea

Oceanic microbial diversity covaries with physicochemical parameters. Temperature, for example, explains approximately half of global variation in surface taxonomic abundance. It is unknown, however, whether covariation patterns hold over narrower parameter gradients and spatial scales, and extending to mesopelagic depths. We collected and sequenced 45 epipelagic and mesopelagic microbial metagenomes on a meridional transect through the eastern Red Sea. We asked which environmental parameters explain the most variation in relative abundances of taxonomic groups, gene ortholog groups, and pathways--at a spatial scale of <2000 km, along narrow but well-defined latitudinal and depth-dependent gradients. We also asked how microbes are adapted to gradients and extremes in irradiance, temperature, salinity, and nutrients, examining the responses of individual gene ortholog groups to these parameters. Functional and taxonomic metrics were equally well explained (75-79%) by environmental parameters. However, only functional and not taxonomic covariation patterns were conserved when comparing with an intruding water mass with different physicochemical properties. Temperature explained the most variation in each metric, followed by nitrate, chlorophyll, phosphate, and salinity. That nitrate explained more variation than phosphate suggested nitrogen limitation, consistent with low surface N:P ratios. Covariation of gene ortholog groups with environmental parameters revealed patterns of functional adaptation to the challenging Red Sea environment: high irradiance, temperature, salinity, and low nutrients. Nutrient acquisition gene ortholog groups were anticorrelated with concentrations of their respective nutrient species, recapturing trends previously observed across much larger distances and environmental gradients. This dataset of metagenomic covariation along densely sampled environmental gradients includes online data exploration supplements, serving as a community resource for marine microbial ecology.

Microbiology↗

bioRxiv2016

The Quick and the Dead: Microbial Demography at the Yeast Thermal Limit

The niche of microorganisms is determined by where their populations can expand. Populations can fail to grow because of high death or low birth rates, but these are challenging to measure in microorganisms. We developed a novel technique that enables single cell measurement of age-structured birth and death rates in the budding yeast, Saccharomyces cerevisiae, and used this method to study responses to heat stress in a genetically diverse panel of strains. We find that individual cells show significant heterogeneity in their rates of birth and death during heat stress. Genotype-by-environment effects on processes that regulate asymmetric cell division contribute to this heterogeneity. These lead to either premature senescence or early life mortality during heat stress, and we find that a mitochondrial inheritance defect explains the early life mortality phenotype of one of the strains we studied. This study demonstrates how the interplay of physiology, genetic variation, and environmental variables influences where microbial populations survive and flourish.

Microbiology↗