Kostas Bourtzis

International Atomic Energy Agency (IAEA), Wien, Vienna, Austria

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Publications (108)399.61 Total impact

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    Kostas Bourtzis, Jorge Hendrichs
    BMC Genetics 12/2014; 15 Suppl 2(Suppl 2):I1. DOI:10.1186/1471-2156-15-S2-I1 · 2.36 Impact Factor
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    ABSTRACT: The Bactrocera dorsalis species complex currently harbors approximately 90 different members. The species complex has undergone many revisions in the past decades, and there is still an ongoing debate about the species limits. The availability of a variety of tools and approaches, such as molecular-genomic and cytogenetic analyses, are expected to shed light on the rather complicated issues of species complexes and incipient speciation. The clarification of genetic relationships among the different members of this complex is a prerequisite for the rational application of sterile insect technique (SIT) approaches for population control. Colonies established in the Insect Pest Control Laboratory (IPCL) (Seibersdorf, Vienna), representing five of the main economic important members of the Bactrocera dorsalis complex were cytologically characterized. The taxa under study were B. dorsalis s.s., B. philippinensis, B. papayae, B. invadens and B. carambolae. Mitotic and polytene chromosome analyses did not reveal any chromosomal characteristics that could be used to distinguish between the investigated members of the B. dorsalis complex. Therefore, their polytene chromosomes can be regarded as homosequential with the reference maps of B. dorsalis s.s.. In situ hybridization of six genes further supported the proposed homosequentiallity of the chromosomes of these specific members of the complex. The present analysis supports that the polytene chromosomes of the five taxa under study are homosequential. Therefore, the use of the available polytene chromosome maps for B. dorsalis s.s. as reference maps for all these five biological entities is proposed. Present data provide important insight in the genetic relationships among the different members of the B. dorsalis complex, and, along with other studies in the field, can facilitate SIT applications targeting this complex. Moreover, the availability of 'universal' reference polytene chromosome maps for members of the complex, along with the documented application of in situ hybridization, can facilitate ongoing and future genome projects in this complex.
    BMC Genetics 12/2014; 15 Suppl 2:S16. DOI:10.1186/1471-2156-15-S2-S16 · 2.36 Impact Factor
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    ABSTRACT: The Anopheles arabiensis genetic sexing strain ANO IPCL1 was developed based on a dieldrin resistant mutation. The strain has been shown to be practical and reliable in terms of female elimination by dieldrin treatments at larval stages, but has provided some difficulties when treatments were applied at the egg stage. The high natural sterility of this strain has advantages and disadvantages in both mass rearing and the sterilisation process. In addition, its recombination rate, although relatively low, poses a threat of strain deterioration if left unchecked in a mass-rearing setting. The males of the ANO IPCL1 have been shown to be equally competitive as lab-reared males of the wild-type Dongola strain, but competitiveness decreased by half when irradiated with 75 Gy - a dose conferring >98% sterility. More controversial issues surround the use of dieldrin - a highly persistent organochlorine that is known to bioaccumulate in the food chain. The prospective use of large volumes of dieldrin in a mass-rearing facility and the retention of its residues by the male mosquitoes makes the use of the strain in the context of the sterile insect technique against this vector highly questionable, and therefore its implementation at a large scale cannot be recommended.
    Acta Tropica 11/2014; DOI:10.1016/j.actatropica.2014.11.013 · 2.52 Impact Factor
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    ABSTRACT: Cydia splendana and C. fagiglandana are two closely related chestnut feeding lepidopteran moth species. In this study, we surveyed the bacterial endosymbiont Wolbachia in these two species. Infection rates were 31% in C. splendana and 77% in C. fagiglandana. MLST analysis showed that these two species are infected with two quite diverse Wolbachia strains. C. splendana with Sequence Type (ST) 409 from the A-supergroup and C. fagiglandana with ST 150 from the B-supergroup. One individual of C. splendana was infected with ST 150, indicating horizontal transfer between these sister species. The mitochondrial DNA of the two Cydia species showed a significantly different mtDNA diversity, which was inversely proportional to their infection rates.
    PLoS ONE 11/2014; 9(11). DOI:10.1371/journal.pone.0112795 · 3.53 Impact Factor
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    ABSTRACT: Bactrocera papayae Drew & Hancock, Bactrocera philippinensis Drew & Hancock, Bactrocera carambolae Drew & Hancock, and Bactrocera invadens Drew, Tsuruta & White are four horticultural pest tephritid fruit fly species that are highly similar, morphologically and genetically, to the destructive pest, the Oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). This similarity has rendered the discovery of reliable diagnostic characters problematic, which, in view of the economic importance of these taxa and the international trade implications, has resulted in ongoing difficulties for many areas of plant protection and food security. Consequently, a major international collaborative and integrated multidisciplinary research effort was initiated in 2009 to build upon existing literature with the specific aim of resolving biological species limits among B. papayae, B. philippinensis, B. carambolae, B. invadens and B. dorsalis to overcome constraints to pest management and international trade. Bactrocera philippinensis has recently been synonymized with B. papayae as a result of this initiative and this review corroborates that finding; however, the other names remain in use. While consistent characters have been found to reliably distinguish B. carambolae from B. dorsalis, B. invadens and B. papayae, no such characters have been found to differentiate the latter three putative species. We conclude that B. carambolae is a valid species and that the remaining taxa, B. dorsalis, B. invadens and B. papayae, represent the same species. Thus, we consider B. dorsalis (Hendel) as the senior synonym of B. papayae Drew and Hancock syn.n. and B. invadens Drew, Tsuruta & White syn.n. A redescription of B. dorsalis is provided. Given the agricultural importance of B. dorsalis, this taxonomic decision will have significant global plant biosecurity implications, affecting pest management, quarantine, international trade, postharvest treatment and basic research. Throughout the paper, we emphasize the value of independent and multidisciplinary tools in delimiting species, particularly in complicated cases involving morphologically cryptic taxa.
    Systematic Entomology 10/2014; DOI:10.1111/syen.12113 · 2.55 Impact Factor
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    ABSTRACT: In the last decade, bacterial symbionts have been shown to play an important role in protecting hosts against pathogens. Wolbachia, a widespread symbiont in arthropods, can protect Drosophila and mosquito species against viral infections. We have investigated antiviral protection in 19 Wolbachia strains originating from 16 Drosophila species after transfer into the same genotype of Drosophila simulans. We found that approximately half of the strains protected against two RNA viruses. Given that 40% of terrestrial arthropod species are estimated to harbour Wolbachia, as many as a fifth of all arthropods species may benefit from Wolbachia-mediated protection. The level of protection against two distantly related RNA viruses – DCV and FHV – was strongly genetically correlated, which suggests that there is a single mechanism of protection with broad specificity. Furthermore, Wolbachia is making flies resistant to viruses, as increases in survival can be largely explained by reductions in viral titer. Variation in the level of antiviral protection provided by different Wolbachia strains is strongly genetically correlated to the density of the bacteria strains in host tissues. We found no support for two previously proposed mechanisms of Wolbachia-mediated protection — activation of the immune system and upregulation of the methyltransferase Dnmt2. The large variation in Wolbachia's antiviral properties highlights the need to carefully select Wolbachia strains introduced into mosquito populations to prevent the transmission of arboviruses.
    PLoS Pathogens 09/2014; 10(9). DOI:10.1371/journal.ppat.1004369 · 8.06 Impact Factor
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    ABSTRACT: Many species of tsetse flies are infected by a hytrosavirus that causes salivary gland hypertrophy (SGH) syndrome.Flies with SGH have a reduced fecundity and fertility. Due to the deleterious impact of the salivary gland hypertrophy virus (SGHV) on Glossinapallidipes colonies, several approaches have beeninvestigated to develop a virus management strategy including the exploitation of endogenous microbiota. Tsetse flies harbor three symbiotic bacteria (Wigglesworthiaglossinidia,Sodalis glossinidius and Wolbachia) in addition to trypanosome the causative agent of sleeping sickness disease in human and nagana in livestock. The interaction of the tsetse microbiota (gut bacteria and symbionts) with the SGHV and / or trypanosome is largely unexplored. In the present study, we show that ampicillin treatment of G. pallidipesimpedes the transgeneration transmission of the SGHVsuggesting the involvement of tsetse microbiota in the virus transmission. Quantitative-PCR analysis of wild tsetse flies (mainly G. morsitansmorsitans and G. austeni) clearly indicated a negative interaction between SGHV and Wolbachia: flies heavily infected with Wolbachia presented significantly low viral titers. In addition, injection of GpSGHV into different Wolbachia-infected Glossina speciesdid not result to the transgeneration transmission of SGHV as normally occurs in G. pallidipes colony, which is free of Wolbachia. Taken together, these data suggest that Wolbachia may interfere with the establishment and transmission of this important DNA virus (SGHV), which represents a major hurdle for the application of SIT strategies for the control of tsetse flies and trypanosomosis in sub-Saharan Africa.
    47th Annual Meeting of the Society for Invertebrate Pathology, Mainz, Germany; 08/2014
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    ABSTRACT: Many species of tsetse flies are infected by a hytrosavirus that causes salivary gland hypertrophy (SGH) syndrome. Flies with SGH have a reduced fecundity and fertility. Due to the deleterious impact of the salivary gland hypertrophy virus (SGHV) on Glossina pallidipes colonies, several approaches have been investigated to develop a virus management strategy including the exploitation of endogenous microbiota. Tsetse flies harbor three symbiotic bacteria (Wigglesworthia glossinidia, Sodalis glossinidius and Wolbachia) in addition to trypanosome the causative agent of sleeping sickness disease in human and nagana in livestock. The interaction of the tsetse microbiota (gut bacteria and symbionts) with the SGHV and / or trypanosome is largely unexplored. In the present study, we show that ampicillin treatment of G. pallidipes impedes the transgeneration transmission of the SGHV suggesting the involvement of tsetse microbiota in the virus transmission. Quantitative- PCR analysis of wild tsetse flies (mainly G. morsitans morsitans and G. austeni) clearly indicated a negative interaction between SGHV and Wolbachia: flies heavily infected with Wolbachia presented significantly low viral titers. In addition, injection of GpSGHV into different Wolbachia-infected Glossina species did not result to the transgeneration transmission of SGHV as normally occurs in G. pallidipes colony, which is free of Wolbachia. Taken together, these data suggest that Wolbachia may interfere with the establishment and transmission of this important DNA virus (SGHV), which represents a major hurdle for the application of SIT strategies for the control of tsetse flies and trypanosomosis in sub-Saharan Africa.
    Societyfor Invertebrate Pathology Meeting in 2014, Mainz, Germany.; 08/2014
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    ABSTRACT: Rhagoletis cerasi (Diptera: Tephritidae) is a major pest of sweet and sour cherries in Europe and parts of Asia. Despite its economic significance, there is a lack of studies on the genetic structure of R. cerasi populations. Elucidating the genetic structure of insects of economic importance is crucial for developing phenological-predictive models and environmental friendly control methods. All natural populations of R. cerasi have been found to harbor the endosymbiont Wolbachia pipientis, which widely affects multiple biological traits contributing to the evolution of its hosts, and has been suggested as a tool for the biological control of insect pests and disease vectors. In the current study, the analysis of 18 R. cerasi populations collected in Greece, Germany, and Russia using 13 microsatellite markers revealed structuring of R. cerasi natural populations, even at close geographic range. We also analyzed the Wolbachia infection status of these populations using 16S rRNA-, MLST- and wsp-based approaches. All 244 individuals screened were positive for Wolbachia. Our results suggest the fixation of the wCer1 strain in Greece while wCer2, wCer4, wCer5, and probably other uncharacterized strains were also detected in multiply infected individuals. The role of Wolbachia and its potential extended phenotypes needs a thorough investigation in R. cerasi. Our data suggest an involvement of this symbiont in the observed restriction in the gene flow in addition to a number of different ecological factors.
    Ecology and Evolution 05/2014; 4(10). DOI:10.1002/ece3.553 · 1.66 Impact Factor
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    ABSTRACT: Tsetse flies are the sole vectors of human African trypanosomiasis throughout sub-Saharan Africa. Both sexes of adult tsetse feed exclusively on blood and contribute to disease transmission. Notable differences between tsetse and other disease vectors include obligate microbial symbioses, viviparous reproduction, and lactation. Here, we describe the sequence and annotation of the 366-megabase Glossina morsitans morsitans genome. Analysis of the genome and the 12,308 predicted protein-encoding genes led to multiple discoveries, including chromosomal integrations of bacterial (Wolbachia) genome sequences, a family of lactation-specific proteins, reduced complement of host pathogen recognition proteins, and reduced olfaction/chemosensory associated genes. These genome data provide a foundation for research into trypanosomiasis prevention and yield important insights with broad implications for multiple aspects of tsetse biology.
    Science 04/2014; 344(6182):380-386. · 31.48 Impact Factor
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    ABSTRACT: Tsetse flies are the sole vectors of human African trypanosomiasis throughout sub-Saharan Africa. Both sexes of adult tsetse feed exclusively on blood and contribute to disease transmission. Notable differences between tsetse and other disease vectors include obligate microbial symbioses, viviparous reproduction, and lactation. Here, we describe the sequence and annotation of the 366-megabase Glossina morsitans morsitans genome. Analysis of the genome and the 12,308 predicted protein–encoding genes led to multiple discoveries, including chromosomal integrations of bacterial (Wolbachia) genome sequences, a family of lactation-specific proteins, reduced complement of host pathogen recognition proteins, and reduced olfaction/chemosensory associated genes. These genome data provide a foundation for research into trypanosomiasis prevention and yield important insights with broad implications for multiple aspects of tsetse biology.
    Science 04/2014; 344:380. DOI:10.1126/science.1249656 · 31.48 Impact Factor
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    ABSTRACT: Tsetse flies (Glossina spp.) are the cyclical vectors of Trypanosoma spp., which are unicellular parasites responsible for multiple diseases, including nagana in livestock and sleeping sickness in humans in Africa. Glossina species, including Glossina morsitans morsitans (Gmm), for which the Whole Genome Sequence (WGS) is now available, have established symbiotic associations with three endosymbionts: Wigglesworthia glossinidia, Sodalis glossinidius and Wolbachia pipientis (Wolbachia). The presence of Wolbachia in both natural and laboratory populations of Glossina species, including the presence of horizontal gene transfer (HGT) events in a laboratory colony of Gmm, has already been shown. We herein report on the draft genome sequence of the cytoplasmic Wolbachia endosymbiont (cytWol) associated with Gmm. By in silico and molecular and cytogenetic analysis, we discovered and validated the presence of multiple insertions of Wolbachia (chrWol) in the host Gmm genome. We identified at least two large insertions of chrWol, 527,507 and 484,123 bp in size, from Gmm WGS data. Southern hybridizations confirmed the presence of Wolbachia insertions in Gmm genome, and FISH revealed multiple insertions located on the two sex chromosomes (X and Y), as well as on the supernumerary B-chromosomes. We compare the chrWol insertions to the cytWol draft genome in an attempt to clarify the evolutionary history of the HGT events. We discuss our findings in light of the evolution of Wolbachia infections in the tsetse fly and their potential impacts on the control of tsetse populations and trypanosomiasis.
    PLoS Neglected Tropical Diseases 04/2014; 8(4):e2728. DOI:10.1371/journal.pntd.0002728 · 4.49 Impact Factor
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    ABSTRACT: Mosquito species, members of the genera Aedes, Anopheles and Culex, are the major vectors of human pathogens including protozoa (Plasmodium spp.), filariae and of a variety of viruses (causing dengue, chikungunya, yellow fever, West Nile). There is lack of efficient methods and tools to treat many of the diseases caused by these major human pathogens, since no efficient vaccines or drugs are available; even in malaria where insecticide use and drug therapies have reduced incidence, 219 million cases still occurred in 2010. Therefore efforts are currently focused on the control of vector populations. Insecticides alone are insufficient to control mosquito populations since reduced susceptibility and even resistance is being observed more and more frequently. There is also increased concern about the toxic effects of insecticides on non-target (even beneficial) insect populations, on humans and the environment. During recent years, the role of symbionts in the biology, ecology and evolution of insect species has been well-documented and has led to suggestions that they could potentially be used as tools to control pests and therefore diseases. Wolbachia is perhaps the most renowned insect symbiont, mainly due to its ability to manipulate insect reproduction and to interfere with major human pathogens thus providing new avenues for pest control. We herein present recent achievements in the field of mosquito-Wolbachia symbiosis with an emphasis on Aedes albopictus. We also discuss how Wolbachia symbiosis can be harnessed for vector control as well as the potential to combine the sterile insect technique and Wolbachia-based approaches for the enhancement of population suppression programs.
    Acta tropica 11/2013; 132. DOI:10.1016/j.actatropica.2013.11.004 · 2.52 Impact Factor
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    Spyridon Ntougias, Kostas Bourtzis, George Tsiamis
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    ABSTRACT: Olive mill wastes (OMWs) are high-strength organic effluents, which upon disposal can degrade soil and water quality, negatively affecting aquatic and terrestrial ecosystems. The main purpose of this review paper is to provide an up-to-date knowledge concerning the microbial communities identified over the past 20 years in olive mill wastes using both culture-dependent and independent approaches. A database survey of 16S rRNA gene sequences (585 records in total) obtained from olive mill waste environments revealed the dominance of members of Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, Firmicutes, and Actinobacteria. Independent studies confirmed that OMW microbial communities' structure is cultivar dependant. On the other hand, the detection of fecal bacteria and other potential human pathogens in OMWs is of major concern and deserves further examination. Despite the fact that the degradation and detoxification of the olive mill wastes have been mostly investigated through the application of known bacterial and fungal species originated from other environmental sources, the biotechnological potential of indigenous microbiota should be further exploited in respect to olive mill waste bioremediation and inactivation of plant and human pathogens. The implementation of omic and metagenomic approaches will further elucidate disposal issues of olive mill wastes.
    10/2013; 2013:784591. DOI:10.1155/2013/784591
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    ABSTRACT: Tsetse flies (Diptera: Glossinidae) harbour three known vertically transmitted bacterial symbionts (Wigglesworthia, Sodalis, and/or Wolbachia) that modulate the reproduction and immune competence of the flies. Wigglesworthia and Sodalis are both intra- and extra-cellular, while Wolbachia is strictly intracellular. Wigglesworthia resides in the midgut bacteriocytes or in the milk glands and does not infect reproductive tissues. Sodalis resides in the reproductive tract and infects the mid-guts, hemolymph and milk glands, while Wolbachia exclusively infects germ tissues. Some tsetse species such as G. pallidipes also harbour Glossina pallidipes salivary gland hypertrophy virus (GpSGHV), whose infection phenotypes can be either asymptomatic or symptomatic. In mosquitoes, aphids and tsetse the removal of the symbionts by antibiotics impacts host fitness and increases host susceptibility to pathogen infections. We therefore hypothesized that suppression of the G. pallidipes symbionts would alter GpSGHV titres and/or expression of salivary gland hypertrophy (SGH) in parent and their progenies. Injected virus replicated in the parents, but was not secreted via saliva during fly feeding. Whereas GpSGHV-injected parents did not exhibit SGH, the incidence of SGH symptoms increased from 4.5% to > 95% from the first to the fourth larviposition cycles of the F1 progenies. Ampicillin had negligible impacts on the virus titres in adult parents. However, the antibiotic reduced titres of GpSGHV, Sodalis and Wigglesworthia, and negated expression of SGH symptoms in the F1 progenies. Wolbachia was not detected in any of the analysed samples. The results indicated that the fat body tracheal system may provide a conduit for the trans-generational GpSGHV transmission via milk gland secretions, and that the removal of the microbiome suppresses this transmission. These data suggest that the G. pallidipes microbiome may have co-evolved with GpSGHV, and plays key roles in the mother-to-progeny transmission of the virus.
    EFS-EMBO Symposium; Integrated insect immunology: From basic biology to environmental applications, Polonia Castle in Pultusk, Poland; 09/2013
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    ABSTRACT: Etoliko, an anoxic semi-enclosed basin, is part of a complex wetland in Western Greece extremely rich in biodiversity. It covers an area of 1,700 ha with an atypical orientation that has been formed tectonically. In order to identify the main factors influencing the bacterial profile at the Etoliko basin, 48 samples were collected, representing seasonal variation at four sampling stations. Physico-chemical analysis of the samples indicates the presence of three layers in the Etoliko basin: (1) low-density surface layer, (2) a layer with a steep density gradient, and (3) dense water below a depth of 20 m. A permanent halocline, whose thickness is varying seasonally, has been identified in the Etoliko basin water column, while the spatiotemporal salinity distribution was highly affected by the basin’s interaction with the nearby Messolonghi lagoon. The anoxic zone extends from 20 m below the surface to the bottom of the Etoliko basin in summer, while the bottom layer was hypoxic during winter. Bacterial populations were analyzed by Automated Ribosomal Intergenic Spacer Analysis (ARISA). Bacterial richness and diversity were calculated and compared across samples. Hierarchical analysis showed that ARISA clustered the surface water samples according to seasonal variation, while sediment and near-to-bottom water samples appear to be stable and to cluster together. Non-metric multidimensional scaling (MDS) indicates that bacterial composition depends on dissolved oxygen and salinity. Increase in salinity of the ecosystem leads to a significant reduction of the microbial diversity.
    Annals of Microbiology 09/2013; 64(2). DOI:10.1007/s13213-013-0700-3 · 1.04 Impact Factor
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    ABSTRACT: When considering a mosquito release programme, one of the first issues to be addressed is how to eliminate/separate the females. The greatest number of options might eventually be available for those who can use transgenic mosquitoes, but the inherent characteristics of the target species may also provide possibilities for interim measures until more efficient methods can be developed. Differences in intrinsic size, in behaviour and in development rate between females and males are often available and useful for sexing. Efficient species-specific systems for eliminating females at the embryo stage have been developed, but most have since been discarded due to lack of use. Ideal systems specifically kill female embryos using some treatment that can be manipulated during production. Such killing systems are far more efficient than using intrinsic sexual differences, but they systems require selectable genetic markers and sex-linkage created by rare random chromosomal rearrangements. While intrinsic sexual differences should not be considered as long-term candidates for the development of robust and efficient sexing approaches, in the absence of these, the accessibility and integration of less efficient systems can provide a stop-gap measure that allows rapid start up with a minimum of investment. The International Atomic Energy Agency is funding over a 5 year period (2013-2018) a new Coordinated Research Project on "Exploring Genetic, Molecular, Mechanical and Behavioural Methods of Sex Separation in Mosquitoes" to network researchers and to address the critical need of genetic sexing strains for the implementation of the sterile insect technique (using radiation-sterilised or transgenic male mosquitoes) and for insect incompatibility technique programmes against disease-transmitting mosquitoes.
    Acta tropica 08/2013; DOI:10.1016/j.actatropica.2013.08.015 · 2.52 Impact Factor
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    Spyridon Ntougias, Kostas Bourtzis, George Tsiamis
    [Show abstract] [Hide abstract]
    ABSTRACT: Olive mill wastes (OMWs) are high-strength organic effluents, which upon disposal can degrade soil and water quality, negatively affecting aquatic and terrestrial ecosystems. The main purpose of this review paper is to provide an up-to-date knowledge concerning the microbial communities identified over the past 20 years in olive mill wastes using both culture-dependent and independent approaches. A database survey of 16S rRNA gene sequences (585 records in total) obtained from olive mill waste environments revealed the dominance of members of Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria, Firmicutes, and Actinobacteria. Independent studies confirmed that OMW microbial communities' structure is cultivar dependant. On the other hand, the detection of fecal bacteria and other potential human pathogens in OMWs is of major concern and deserves further examination. Despite the fact that the degradation and detoxification of the olive mill wastes have been mostly investigated through the application of known bacterial and fungal species originated from other environmental sources, the biotechnological potential of indigenous microbiota should be further exploited in respect to olive mill waste bioremediation and inactivation of plant and human pathogens. The implementation of omic and metagenomic approaches will further elucidate disposal issues of olive mill wastes.

Publication Stats

3k Citations
399.61 Total Impact Points

Institutions

  • 2014
    • International Atomic Energy Agency (IAEA)
      • FAO/IAEA Agriculture and Biotechnology Laboratories
      Wien, Vienna, Austria
  • 2011–2014
    • University of Western Greece
      Agrínio, West Greece, Greece
  • 1989–2014
    • University of Patras
      • • Department of Environmental and Natural Resources Management
      • • Department of Biology
      • • Division of Genetics, Cell and Developmental Biology
      Rhion, West Greece, Greece
  • 2011–2012
    • Biomedical Sciences Research Center Alexander Fleming
      Βάρη, Attica, Greece
  • 1970–2012
    • University of Ioannina
      • Department of Environmental and Natural Resources Management
      Yannina, Epirus, Greece
  • 2010
    • Università degli Studi di Modena e Reggio Emilia
      Modène, Emilia-Romagna, Italy
    • Bielefeld University
      Bielefeld, North Rhine-Westphalia, Germany
  • 2009
    • University of Pavia
      Ticinum, Lombardy, Italy
  • 2004
    • University of Illinois at Chicago
      Chicago, Illinois, United States
    • Institut Jacques Monod
      Lutetia Parisorum, Île-de-France, France
  • 1994–2004
    • Foundation for Research and Technology - Hellas
      • Institute of Molecular Biology and Biotechnology (IMBB)
      Megalokastro, Crete, Greece
    • Institute of Genetics and Molecular Medicine
      Edinburgh, Scotland, United Kingdom
  • 1999–2001
    • Yale-New Haven Hospital
      New Haven, Connecticut, United States
  • 1998
    • Yale University
      New Haven, Connecticut, United States