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Department of Plant Pathology and Microbiology
The Robert H. Smith Faculty of Agriculture, Food & Environment
The Hebrew University of Jerusalem

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2021
Cohen, Y. ; Pasternak, Z. ; Muller, S. ; Hubschmann, T. ; Schattenberg, F. ; Sivakala, K. K. ; Abed-Rabbo, A. ; Chatzinotas, A. ; Jurkevitch, E. Community and single cell analyses reveal complex predatory interactions between bacteria in high diversity systems. NATURE COMMUNICATIONS 2021, 12.Abstract
Studying the role of predator-prey interactions in food-web stability and species coexistence in the environment is arduous. Here, Cohen et al. use a combination of community and single-cell analyses to show that bacterial predators can regulate prey populations in the species-rich environments of wastewater treatment plants. A fundamental question in community ecology is the role of predator-prey interactions in food-web stability and species coexistence. Although microbial microcosms offer powerful systems to investigate it, interrogating the environment is much more arduous. Here, we show in a 1-year survey that the obligate predators Bdellovibrio and like organisms (BALOs) can regulate prey populations, possibly in a density-dependent manner, in the naturally complex, species-rich environments of wastewater treatment plants. Abundant as well as rarer prey populations are affected, leading to an oscillating predatory landscape shifting at various temporal scales in which the total population remains stable. Shifts, along with differential prey range, explain co-existence of the numerous predators through niche partitioning. We validate these sequence-based findings using single-cell sorting combined with fluorescent hybridization and community sequencing. Our approach should be applicable for deciphering community interactions in other systems.
Slipko, K. ; Marano, R. B. M. ; Cytryn, E. ; Merkus, V. ; Wogerbauer, M. ; Krampe, J. ; Jurkevitch, E. ; Kreuzinger, N. Effects of subinhibitory quinolone concentrations on functionality, microbial community composition, and abundance of antibiotic resistant bacteria and qnrS in activated sludge. JOURNAL OF ENVIRONMENTAL CHEMICAL ENGINEERING 2021, 9.Abstract
Wastewater treatment plants (WWTPs) are continuously exposed to sub-inhibitory concentrations of antibiotics that are thought to contribute to the spreading of antibiotic resistant bacteria and antibiotic resistance genes, which are eventually released to downstream environments through effluents. In order to understand the effects of sub-inhibitory concentrations of antibiotics on sludge microbiome and resistome, we spiked a conventional activated sludge (CAS) model system with ciprofloxacin, a common fluoroquinolone antibiotic, from 0.0001 mg/L (about twice the typical ciprofloxacin concentration observed in municipal wastewater) up to 0.1 mg/L (one order of magnitude below the clinical MIC for Enterobacteriaceae) for 151 days. The abundance of ciprofloxacin resistant bacteria and qnrS, a plasmid-associated gene that confers resistance to quinolones, in activated sludge and in effluents of control and spiked CAS reactors, showed no measurable effect of the antibiotic amendment. This was also true for the bacterial community structure and for indicators of WW treatment such as N removal efficiency. Surprisingly, temporal fluctuations in both reactors could explain the observed internal variability of these antibiotic resistance determinants better than the hypothesized antibiotic-driven selective pressure. Overall, this work shows that the core sludge microbiome in CAS systems is resilient to sub-inhibitory concentrations of ciprofloxacin at a functional, structural, and antibiotic resistance levels.
Marano, R. B. M. ; Gupta, C. L. ; Cozer, T. ; Jurkevitch, E. ; Cytryn, E. Hidden Resistome: Enrichment Reveals the Presence of Clinically Relevant Antibiotic Resistance Determinants in Treated Wastewater-Irrigated Soils. ENVIRONMENTAL SCIENCE & TECHNOLOGY 2021, 55, 6814-6827.Abstract
Treated-wastewater (TW) irrigation transfers antibiotic-resistant bacteria (ARB) to soil, but persistence of these bacteria is generally low due to resilience of the soil microbiome. Nonetheless, wastewater-derived bacteria and associated antibiotic resistance genes (ARGs) may persist below detection levels and potentially proliferate under copiotrophic conditions. To test this hypothesis, we exposed soils from microcosm, lysimeter, and field experiments to short-term enrichment in copiotroph-stimulating media. In microcosms, enrichment stimulated growth of multidrug-resistant Escherichia coli up to 2 weeks after falling below detection limits. Lysimeter and orchard soils irrigated in-tandem with either freshwater or TW were subjected to culture-based, qPCR and shotgun metagenomic analyses prior, and subsequent, to enrichment. Although native TW- and freshwater-irrigated soil microbiomes and resistomes were similar to each other, enrichment resulted in higher abundances of cephalosporin- and carbapenem-resistant Enterobacteriaceae and in substantial differences in the composition of microbial communities and ARGs. Enrichment stimulated ARG-harboring Bacillaceae in the freshwater-irrigated soils, whereas in TWW-irrigated soils, ARG-harboring.-proteobacterial families Enterobacteriaceae and Moraxellaceae were more profuse. We demonstrate that TW-derived ARB and associated ARGs can persist at below detection levels in irrigated soils and believe that similar short-term enrichment strategies can be applied for environmental antimicrobial risk assessment in the future.
Shu, R. ; Hahn, D. A. ; Jurkevitch, E. ; Liburd, O. E. ; Yuval, B. ; Wong, A. C. - N. Sex-Dependent Effects of the Microbiome on Foraging and Locomotion in Drosophila suzukii. FRONTIERS IN MICROBIOLOGY 2021, 12.Abstract
There is growing evidence that symbiotic microbes can influence multiple nutrition-related behaviors of their hosts, including locomotion, feeding, and foraging. However, how the microbiome affects nutrition-related behavior is largely unknown. Here, we demonstrate clear sexual dimorphism in how the microbiome affects foraging behavior of a frugivorous fruit fly, Drosophila suzukii. Female flies deprived of their microbiome (axenic) were consistently less active in foraging on fruits than their conventional counterparts, even though they were more susceptible to starvation and starvation-induced locomotion was notably more elevated in axenic than conventional females. Such behavioral change was not observed in male flies. The lag of axenic female flies but not male flies to forage on fruits is associated with lower oviposition by axenic flies, and mirrored by reduced food seeking observed in virgin females when compared to mated, gravid females. In contrast to foraging intensity being highly dependent on the microbiome, conventional and axenic flies of both sexes showed relatively consistent and similar fruit preferences in foraging and oviposition, with raspberries being preferred among the fruits tested. Collectively, this work highlights a clear sex-specific effect of the microbiome on foraging and locomotion behaviors in flies, an important first step toward identifying specific mechanisms that may drive the modulation of insect behavior by interactions between the host, the microbiome, and food.
Sathyamoorthy, R. ; Kushmaro, Y. ; Rotem, O. ; Matan, O. ; Kadouri, D. E. ; Huppert, A. ; Jurkevitch, E. To hunt or to rest: prey depletion induces a novel starvation survival strategy in bacterial predators. ISME JOURNAL 2021, 15, 109-123.Abstract
The small size of bacterial cells necessitates rapid adaption to sudden environmental changes. InBdellovibrio bacteriovorus, an obligate predator of bacteria common in oligotrophic environments, the non-replicative, highly motile attack phase (AP) cell must invade a prey to ensure replication. AP cells swim fast and respire at high rates, rapidly consuming their own contents. How the predator survives in the absence of prey is unknown. We show that starvation for prey significantly alters swimming patterns and causes exponential decay in prey-searching cells over hours, until population-wide swim-arrest. Swim-arrest is accompanied by changes in energy metabolism, enabling rapid swim-reactivation upon introduction of prey or nutrients, and a sweeping change in gene expression and gene regulation that largely differs from those of the paradigmatic stationary phase. Swim-arrest is costly as it imposes a fitness penalty in the form of delayed growth. We track the control of the swim arrest-reactivation process to cyclic-di-GMP (CdG) effectors, including two motility brakes. CRISPRi transcriptional inactivation, and in situ localization of the brakes to the cell pole, demonstrated their essential role for effective survival under prey-induced starvation. Thus, obligate predators evolved a unique CdG-controlled survival strategy, enabling them to sustain their uncommon lifestyle under fluctuating prey supply.
Sathyamoorthy, R. ; Huppert, A. ; Kadouri, D. E. ; Jurkevitch, E. Effects of the prey landscape on the fitness of the bacterial predators Bdellovibrio and like organisms. FEMS MICROBIOLOGY ECOLOGY 2021, 97.Abstract
Bdellovibrio and like organisms (BALOs) are obligate predatory bacteria commonly encountered in the environment. In dual predator-prey cultures, prey accessibility ensures optimal feeding and replication and rapid BALO population growth. However, the environmental prey landscape is complex, as it also incorporates non-prey cells and other particles. These may act as decoys, generating unproductive encounters which in turn may affect both predator and prey population dynamics. In this study, we hypothesized that increasing decoy:prey ratios would bring about increasing costs on the predator's reproductive fitness. We also tested the hypothesis that different BALOs and decoys would have different effects. To this end, we constructed prey landscapes including petiplasmic or epibiotic predators including two types of decoy under a large range of initial decoy:prey ratio, and mixed cultures containing multiple predators and prey. We show that as decoy:prey ratios increase, the maximal predator population sizes is reduced and the time to reach it significantly increases. We found that BALOs spent less time handling non-prey (including superinfection-immune invaded prey) than prey cells, and did not differentiate between efficient and less efficient prey. This may explain why in multiple predator and prey cultures, less preferred prey appear to act as decoy.
Sivakala, K. K. ; Jose, P. A. ; Matan, O. ; Zohar-Perez, C. ; Nussinovitch, A. ; Jurkevitch, E. In vivo predation and modification of the Mediterranean fruit fly Ceratitis capitata (Wiedemann) gut microbiome by the bacterial predator Bdellovibrio bacteriovorus. JOURNAL OF APPLIED MICROBIOLOGY 2021, 131, 2971-2980.Abstract
Aims The Mediterranean fruit fly (the medfly) causes major losses of agricultural fruits. Its microbiome is mainly composed of various Enterobacteriaceae that contribute to nutrient acquisition and are associated with the fly's development. Moreover, the performance of males produced by the sterile insect technique is improved by providing mass-reared insects with specific gut bacteria. Bdellovibrio and like organisms (BALOs) are obligate predators of Gram-negative bacteria that efficiently preys upon diverse Enterobacteriaceae, making it a potential disruptor of the fly's microbiome. We hypothesized that the fly's microbiome can be targeted to control the insect. Methods and Results Inoculation of B. bacteriovorus as free-swimming or encapsulated cells into gut extracts significantly reduced gut bacterial abundance, sustaining predator survival. Similar treatments applied to adult flies showed that the predators also survived in the gut environment. While addition of the predators did not affect total gut bacterial abundance and end-point fly mortality, a shift in the gut community structure, measured by high-throughput community sequencing was observed. Conclusions The bacterial predator of bacteria B. bacteriovorus can prey and survive in vivo in the medfly gut. Significance and Impact of the Study This study establishes the potential of BALOs to affect the microbiome of insect hosts.
Mookherjee, A. ; Jurkevitch, E. Interactions between Bdellovibrio and like organisms and bacteria in biofilms: beyond predator-prey dynamics. ENVIRONMENTAL MICROBIOLOGY 2021.Abstract
Bdellovibrio and like organisms (BALOs) prey on Gram-negative bacteria in the planktonic phase as well as in biofilms, with the ability to reduce prey populations by orders of magnitude. During the last few years, evidence has mounted for a significant ecological role for BALOs, with important implications for our understanding of microbial community dynamics as well as for applications against pathogens, including drug-resistant pathogens, in medicine, agriculture and aquaculture, and in industrial settings for various uses. However, our understanding of biofilm predation by BALOs is still very fragmentary, including gaps in their effect on biofilm structure, on prey resistance, and on evolutionary outcomes of both predators and prey. Furthermore, their impact on biofilms has been shown to reach beyond predation, as they are reported to reduce biofilm structures of non-prey cells (including Gram-positive bacteria). Here, we review the available literature on BALOs in biofilms, extending known aspects to potential mechanisms employed by the predators to grow in biofilms. Within that context, we discuss the potential ecological significance and potential future utilization of the predatory and enzymatic possibilities offered by BALOs in medical, agricultural and environmental applications.
Jose, P. A. ; Ben-Yosef, M. ; Lahuatte, P. ; Causton, C. E. ; Heimpel, G. E. ; Jurkevitch, E. ; Yuval, B. Shifting microbiomes complement life stage transitions and diet of the bird parasite Philornis downsi from the Galapagos Islands. ENVIRONMENTAL MICROBIOLOGY 2021, 23, 5014-5029.Abstract
Domestication disconnects an animal from its natural environment and diet, imposing changes in the attendant microbial community. We examine these changes in Philornis downsi (Muscidae), an invasive parasitic fly of land birds in the Galapagos Islands. Using a 16S rDNA profiling approach we studied the microbiome of larvae and adults of wild and laboratory-reared populations. These populations diverged in their microbiomes, significantly more so in larval than in adult flies. In field-collected second-instar larvae, Klebsiella (70.3%) was the most abundant taxon, while in the laboratory Ignatzschineria and Providencia made up 89.2% of the community. In adults, Gilliamella and Dysgonomonas were key members of the core microbiome of field-derived females and males but had no or very low representation in the laboratory. Adult flies harbour sex-specific microbial consortia in their gut, as male core microbiomes were significantly dominated by Klebsiella. Thus, P. downsi microbiomes are dynamic and shift correspondingly with life cycle and diet. Sex-specific foraging behaviour of adult flies and nest conditions, which are absent in the laboratory, may contribute to shaping distinct larval, and adult male and female microbiomes. We discuss these findings in the context of microbe-host co-evolution and the implications for control measures.
Jurkevitch, E. ; Pasternak, Z. A walk on the dirt: soil microbial forensics from ecological theory to the crime lab. FEMS MICROBIOLOGY REVIEWS 2021, 45.Abstract
Forensics aims at using physical evidence to solve investigations with science-based principles, thus operating within a theoretical framework. This however is often rather weak, the exception being DNA-based human forensics that is well anchored in theory. Soil is a most commonly encountered, easily and unknowingly transferred evidence but it is seldom employed as soil analyses require extensive expertise. In contrast, comparative analyses of soil bacterial communities using nucleic acid technologies can efficiently and precisely locate the origin of forensic soil traces. However, this application is still in its infancy, and is very rarely used. We posit that understanding the theoretical bases and limitations of their uses is essential for soil microbial forensics to be judiciously implemented. Accordingly, we review the ecological theory and experimental evidence explaining differences between soil microbial communities, i.e. the generation of beta diversity, and propose to integrate a bottom-up approach of interactions at the microscale, reflecting historical contingencies with top-down mechanisms driven by the geographic template, providing a potential explanation as to why bacterial communities map according to soil types. Finally, we delimit the use of soil microbial forensics based on the present technologies and ecological knowledge, and propose possible venues to remove existing bottlenecks.
2020
Marano, R. B. M. ; Fernandes, T. ; Manaia, C. M. ; Nunes, O. ; Morrison, D. ; Berendonk, T. U. ; Kreuzinger, N. ; Telson, T. ; Corno, G. ; Fatta-Kassinos, D. ; et al. A global multinational survey of cefotaxime-resistant coliforms in urban wastewater treatment plants. ENVIRONMENT INTERNATIONAL 2020, 144.Abstract
The World Health Organization Global Action Plan recommends integrated surveillance programs as crucial strategies for monitoring antibiotic resistance. Although several national surveillance programs are in place for clinical and veterinary settings, no such schemes exist for monitoring antibiotic-resistant bacteria in the environment. In this transnational study, we developed, validated, and tested a low-cost surveillance and easy to implement approach to evaluate antibiotic resistance in wastewater treatment plants (WWTPs) by targeting cefotaxime-resistant (CTX-R) coliforms as indicators. The rationale for this approach was: i) coliform quantification methods are internationally accepted as indicators of fecal contamination in recreational waters and are therefore routinely applied in analytical labs; ii) CTX-R coliforms are clinically relevant, associated with extended-spectrum beta-lactamases (ESBLs), and are rare in pristine environments. We analyzed 57 WWTPs in 22 countries across Europe, Asia, Africa, Australia, and North America. CTX-R coliforms were ubiquitous in raw sewage and their relative abundance varied significantly (< 0.1% to 38.3%), being positively correlated (p < 0.001) with regional atmospheric temperatures. Although most WWTPs removed large proportions of CTX-R coliforms, loads over 10(3) colony-forming units per mL were occasionally observed in final effluents. We demonstrate that CTX-R coliform monitoring is a feasible and affordable approach to assess wastewater antibiotic resistance status.
Dror, B. ; Wang, Z. ; Brady, S. F. ; Jurkevitch, E. ; Cytryn, E. Elucidating the Diversity and Potential Function of Nonribosomal Peptide and Polyketide Biosynthetic Gene Clusters in the Root Microbiome. MSYSTEMS 2020, 5.Abstract
Polyketides (PKs) and nonribosomal peptides (NRPs) are two microbial secondary metabolite (SM) families known for their variety of functions, including antimicrobials, siderophores, and others. Despite their involvement in bacterium-bacterium and bacterium-plant interactions, root-associated SMs are largely unexplored due to the limited cultivability of bacteria. Here, we analyzed the diversity and expression of SM-encoding biosynthetic gene clusters (BGCs) in root microbiomes by culture-independent amplicon sequencing, shotgun metagenomics, and metatranscriptomics. Roots (tomato and lettuce) harbored distinct compositions of nonribosomal peptide synthetases (NRPSs) and polyketide synthases (PKSs) relative to the adjacent bulk soil, and specific BGC markers were both enriched and highly expressed in the root microbiomes. While several of the highly abundant and expressed sequences were remotely associated with known BGCs, the low similarity to characterized genes suggests their potential novelty. Low-similarity genes were screened against a large set of soil-derived cosmid libraries, from which five whole BGCs of unknown function were retrieved. Three clusters were taxonomically affiliated with Actinobacteria, while the remaining were not associated with known bacteria. One Streptomyces-derived BGC was predicted to encode a polyene with potential antifungal activity, while the others were too novel to predict chemical structure. Screening against a suite of metagenomic data sets revealed higher abundances of retrieved clusters in roots and soil samples. In contrast, they were almost completely absent in aquatic and gut environments, supporting the notion that they might play an important role in root ecosystems. Overall, our results indicate that root microbiomes harbor a specific assemblage of undiscovered SMs. IMPORTANCE We identified distinct secondary-metabolite-encoding genes that are enriched (relative to adjacent bulk soil) and expressed in root ecosystems yet almost completely absent in human gut and aquatic environments. Several of the genes were distantly related to genes encoding antimicrobials and siderophores, and their high sequence variability relative to known sequences suggests that they may encode novel metabolites and may have unique ecological functions. This study demonstrates that plant roots harbor a diverse array of unique secondary-metabolite-encoding genes that are highly enriched and expressed in the root ecosystem. The secondary metabolites encoded by these genes might assist the bacteria that produce them in colonization and persistence in the root environment. To explore this hypothesis, future investigations should assess their potential role in interbacterial and bacterium-plant interactions.
Dror, B. ; Jurkevitch, E. ; Cytryn, E. State-of-the-art methodologies to identify antimicrobial secondary metabolites in soil bacterial communities-A review. SOIL BIOLOGY & BIOCHEMISTRY 2020, 147.Abstract
Non-ribosomal peptides (NRPs) and polyketides (PKs) are among the most profuse families of secondary metabolites (SM) produced by bacteria. These compounds are believed to play an important ecological role in microbe-microbe and microbe-plant interactions in soil and roots microbiomes. Over the years, screening of NRPs and PKs in soil bacteria has resulted in high rates of rediscovery, mainly due to challenges associated with bacterial isolation. The quest to expose compounds in the hidden ``unculturable'' fraction of the soil microbiome, and to activate existing and novel SM gene clusters in cultivated bacteria, has facilitated a paradigm shift from traditional isolation-based natural product identification platforms to novel `ecologically inspired' culturing techniques and cutting-edge culture-independent methods. This review provides a comprehensive overview of platforms and applications for studying secondary metabolites in soil and root environments, deliberating the benefits and limitations of the various approaches. Initially, it highlights innovative methodologies to ``culture the unculturable'' to uncover novel soil bacterial SM. Next, it explores ``culture-independent'' platforms for the identification of SM-synthesizing gene clusters through next generation sequencing and bioinformatics. It then evaluates innovative approaches for heterologous expression of metabolites from complex soil environments. Finally, it presents a conceptual integrated pipeline for evaluating the potential function and role of root-associated bacterial SM in suppressive soils that inhibit plant pathogens. This pipeline can be modified to address the ecological role of SM in other soil and root ecosystems, which can ultimately enhance our understanding of microbe-microbe and bacterial-plant interactions.
Youdkes, D. ; Helman, Y. ; Burdman, S. ; Matan, O. ; Jurkevitch, E. Potential Control of Potato Soft Rot Disease by the Obligate Predators Bdellovibrio and Like Organisms. APPLIED AND ENVIRONMENTAL MICROBIOLOGY 2020, 86.Abstract
Bacterial soft rot diseases caused by Pectobacterium spp. and Dickeya spp. affect a wide range of crops, including potatoes, a major food crop. As of today, farmers mostly rely on sanitary practices, water management, and plant nutrition for control. We tested the bacterial predators Bdellovibrio and like organisms (BALOs) to control potato soft rot. BALOs are small, motile predatory bacteria found in terrestrial and aquatic environments. They prey on a wide range of Gram-negative bacteria, including animal and plant pathogens. To this end, BALO strains HD100, 1091, and a Delta merRNA derivative of HD100 were shown to efficiently prey on various rot-causing strains of Pectobacterium and Dickeya solani. BALO control of maceration caused by a highly virulent strain of Pectobacterium carotovorum subsp. brasilense was then tested in situ using a potato slice assay. All BALO strains were highly effective at reducing disease, up to complete prevention. Effectivity was concentration dependent, and BALOs applied before P. carotovorum subsp. brasilense inoculation performed significantly better than those applied after the disease-causing agent, maybe due to in situ consumption of glucose by the prey, as glucose metabolism by live prey bacteria was shown to prevent predation. Dead predators and the supernatant of BALO cultures did not significantly prevent maceration, indicating that predation was the major mechanism for the prevention of the disease. Finally, plastic resistance to predation was affected by prey and predator population parameters, suggesting that population dynamics affect prey response to predation. IMPORTANCE Bacterial soft rot diseases caused by Pectobacterium spp. and Dickeya spp. are among the most important plant diseases caused by bacteria. Among other crops, they inflict large-scale damage to potatoes. As of today, farmers have few options to control them. The bacteria Bdellovibrio and like organisms (BALOs) are obligate predators of bacteria. We tested their potential to prey on Pectobacterium spp. and Dickeya spp. and to protect potato. We show that different BALOs can prey on soft rot-causing bacteria and prevent their growth in situ, precluding tissue maceration. Dead predators and the supernatant of BALO cultures did not significantly prevent maceration, showing that the effect is due to predation. Soft rot control by the predators was concentration dependent and was higher when the predator was inoculated ahead of the prey. As residual prey remained, we investigated what determines their level and found that initial prey and predator population parameters affect prey response to predation.
2019
Petrenko, M. ; Friedman, S. P. ; Fluss, R. ; Pasternak, Z. ; Huppert, A. ; Jurkevitch, E. Spatial heterogeneity stabilizes predator–prey interactions at the microscale while patch connectivity controls their outcome. Environmental Microbiology 2019, n/a. Publisher's VersionAbstract
Summary Natural landscapes are both fragmented and heterogeneous, affecting the distribution of organisms, and their interactions. While predation in homogeneous environments increases the probability of population extinction, fragmentation/heterogeneity promotes coexistence and enhances community stability as shown by experimentation with animals and microorganisms, and supported by theory. Patch connectivity can modulate such effects but how microbial predatory interactions are affected by water-driven connectivity is unknown. In soil, patch habitability by microorganisms, and their connectivity depend upon the water saturation degree (SD). Here, using the obligate bacterial predator Bdellovibrio bacteriovorus, and a Burkholderia prey, we show that soil spatial heterogeneity profoundly affects predatory dynamics, enhancing long-term co-existence of predator and prey in a SD-threshold dependent-manner. However, as patches and connectors cannot be distinguished in these soil matrices, metapopulations cannot be invoked to explain the dynamics of increased persistence. Using a set of experiments combined with statistical and physical models we demonstrate and quantify how under full connectivity, predation is independent of water content but depends on soil microstructure characteristics. In contrast, the SD below which predation is largely impaired corresponds to a threshold below which the water network collapses and water connectivity breaks down, preventing the bacteria to move within the soil matrix.
Marano, R. B. M. ; Zolti, A. ; Jurkevitch, E. ; Cytryn, E. Antibiotic resistance and class 1 integron gene dynamics along effluent, reclaimed wastewater irrigated soil, crop continua: elucidating potential risks and ecological constraints. Water Research 2019, 164. Publisher's VersionAbstract
Reuse of municipal wastewater is a growing global trend, but currently there is lack of consensus regarding the potential dissemination of antibiotic resistance elements by treated wastewater irrigation. We tracked intI1, a proxy for anthropogenic pollution, and an assemblage of antibiotic resistance genes associated with mobile elements and/or wastewater (blaGES, blaOXA2, blaOXA10, blaTEM, blaCTX-M-32 and qnrS) in treated wastewater effluents, effluent stabilization reservoirs, and along irrigation water-soil-crop continua in experimental lysimeters and large-scale commercial fields. While several of the targeted antibiotic resistance genes were profuse in effluents, there was almost no correlation between gene abundance in irrigation water and those detected in soil, and no evidence of systematic gene transfer to irrigated soil or crops. In contrast, soil intI1 abundance correlated strongly to irrigation water levels in lysimeters and sandy field soils, but this was not the case for clay-rich soils or for most of the analyzed crops, suggesting that intI1 may not always be a reliable marker for tracking the impact of treated wastewater irrigation. We hypothesize that “ecological boundaries” expedited by biotic and abiotic factors constrain dissemination of antibiotic resistance elements, and assert that a more holistic perception of these factors is crucial for understanding and managing antibiotic resistance dissemination. © 2019 Elsevier Ltd
Cohen, Y. ; Pasternak, Z. ; Johnke, J. ; Abed-Rabbo, A. ; Kushmaro, A. ; Chatzinotas, A. ; Jurkevitch, E. Bacteria and microeukaryotes are differentially segregated in sympatric wastewater microhabitats. Environmental Microbiology 2019, 21, 1757-1770. Publisher's VersionAbstract
Wastewater purification is mostly performed in activated sludge reactors by bacterial and microeukaryotic communities, populating organic flocs and a watery liquor. While there are numerous molecular community studies of the bacterial fraction, those on microeukaryotes are rare. We performed a year-long parallel 16S rRNA gene and 18S rRNA-gene based analysis of the bacterial and of the microeukaryote communities, respectively, of physically separated flocs and particle-free liquor samples from three WWTPs. This uncovered a hitherto unknown large diversity of microeukaryotes largely composed of potential phagotrophs preferentially feeding on either bacteria or other microeukaryotes. We further explored whether colonization of the microhabitats was selective, showing that for both microbial communities, different but often closely taxonomically and functionally related populations exhibiting different dynamic patterns populated the microhabitats. An analysis of their between plants-shared core populations showed the microeukaryotes to be dispersal limited in comparison to bacteria. Finally, a detailed analysis of a weather-caused operational disruption in one of the plants suggested that the absence of populations common to the floc and liquor habitat may negatively affect resilience and stability. © 2019 Society for Applied Microbiology and John Wiley & Sons Ltd.
Sathyamoorthy, R. ; Maoz, A. ; Pasternak, Z. ; Im, H. ; Huppert, A. ; Kadouri, D. ; Jurkevitch, E. Bacterial predation under changing viscosities. Environmental Microbiology 2019, 21, 2997-3010. Publisher's VersionAbstract
Bdellovibrio and like organisms (BALOs) are largely distributed in soils and in water bodies obligate predators of gram-negative bacteria that can affect bacterial communities. Potential applications of BALOs include biomass reduction, their use against pathogenic bacteria in agriculture, and in medicine as an alternative against antibiotic-resistant pathogens. Such different environments and uses mean that BALOs should be active under a range of viscosities. In this study, the predatory behaviour of two strains of the periplasmic predator B. bacteriovorus and of the epibiotic predator Micavibrio aeruginosavorus was examined in viscous polyvinylpyrrolidone (PVP) solutions at 28 and at 37°C, using fluorescent markers and plate counts to track predator growth and prey decay. We found that at high viscosities, although swimming speed was largely decreased, the three predators reduced prey to levels similar to those of non-viscous suspensions, albeit with short delays. Prey motility and clumping did not affect the outcome. Strikingly, under low initial predator concentrations, predation dynamics were faster with increasing viscosity, an effect that dissipated with increasing predator concentrations. Changes in swimming patterns and in futile predator–predator encounters with viscosity, as revealed by path analysis under changing viscosities, along with possible PVP-mediated crowding effects, may explain the observed phenomena. © 2019 Society for Applied Microbiology and John Wiley & Sons Ltd.
Yuval, B. ; Lahuatte, P. ; Jose, P. A. ; Causton, C. E. ; Jurkevitch, E. ; Kouloussis, N. ; Ben-Yosef, M. Behavioral responses of the invasive fly Philornis downsi to stimuli from bacteria and yeast in the laboratory and the field in the Galapagos Islands. Insects 2019, 10. Publisher's VersionAbstract
Philornis downsi Dodge and Aitken (Diptera: Muscidae) is an avian parasitic fly that has invaded the Galapagos archipelago and exerts an onerous burden on populations of endemic land birds. As part of an ongoing effort to develop tools for the integrated management of this fly, our objective was to determine its long-and short-range responses to bacterial and fungal cues associated with adult P. downsi. We hypothesized that the bacterial and fungal communities would elicit attraction at distance through volatiles, and appetitive responses upon contact. Accordingly, we amplified bacteria from guts of adult field-caught flies and from bird feces, and yeasts from fermenting papaya juice (a known attractant of P. downsi), on selective growth media, and assayed the response of flies to these microbes or their exudates. In the field, we baited traps with bacteria or yeast and monitored adult fly attraction. In the laboratory, we used the proboscis extension response (PER) to determine the sensitivity of males and females to tarsal contact with bacteria or yeast. Long range trapping efforts yielded two female flies over 112 trap-nights (attracted by bacteria from bird feces and from the gut of adult flies). In the laboratory, tarsal contact with stimuli from gut bacteria elicited significantly more responses than did yeast stimuli. We discuss the significance of these findings in context with other studies in the field and identify targets for future work. © 2019 by the authors. Licensee MDPI, Basel, Switzerland.
Akami, M. ; Andongma, A. A. ; Zhengzhong, C. ; Nan, J. ; Khaeso, K. ; Jurkevitch, E. ; Niu, C. - Y. ; Yuval, B. Intestinal bacteria modulate the foraging behavior of the oriental fruit fly Bactrocera dorsalis (Diptera: Tephritidae). PLoS ONE 2019, 14. Publisher's VersionAbstract
The gut microbiome of insects directly or indirectly affects the metabolism, immune status, sensory perception and feeding behavior of its host. Here, we examine the hypothesis that in the oriental fruit fly (Bactrocera dorsalis, Diptera: Tephritidae), the presence or absence of gut symbionts affects foraging behavior and nutrient ingestion. We offered protein-starved flies, symbiotic or aposymbiotic, a choice between diets containing all amino acids or only the non-essential ones. The different diets were presented in a foraging arena as drops that varied in their size and density, creating an imbalanced foraging environment. Suppressing the microbiome resulted in significant changes of the foraging behavior of both male and female flies. Aposymbiotic flies responded faster to the diets offered in experimental arenas, spent more time feeding, ingested more drops of food, and were constrained to feed on time-consuming patches (containing small drops of food), when these offered the full complement of amino acids. We discuss these results in the context of previous studies on the effect of the gut microbiome on host behavior, and suggest that these be extended to the life history dimension. © 2019 Akami et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.