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Health Considerations Regarding Horizontal Transfer of Microbial Transgenes Present in Genetically Modified Crops

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Health Considerations Regarding Horizontal Transfer of Microbial Transgenes Present in Genetically Modified Crops Journal of Biomedicine and Biotechnology • 2005:4 (2005) 326–352 • DOI: 10.1155/JBB.2005.326 RESEARCH ARTICLE Health Considerations Regarding Horizontal Transfer of Microbial Transgenes Present in Genetically Modified Crops Gijs A. Kleter, Ad A. C. M. Peijnenburg, and Henk J. M. Aarts RIKILT, Institute of Food Safety, Wageningen University and Research Center, PO Box 230, 6700AE Wageningen, The Netherlands Received 18 October 2004; revised 30 May 2005; accepted 1 June 2005 The potential effects of horizontal gene transfer on human health are an important item in the safety assessment of genetically mod- ified organisms. Horizontal gene transfer from genetically modified crops to gut microflora most likely occurs with transgenes of microbial origin. The characteristics of microbial transgenes other than antibiotic-resistance genes in market-approved genetically modified crops are reviewed. These characteristics include the microbial source, natural function, function in genetically modified crops, natural prevalence, geographical distribution, similarity to other microbial genes, known horizontal transfer activity, selective conditions and environments for horizontally transferred genes, and potential contribution to pathogenicity and virulence in hu- mans and animals. The assessment of this set of data for each of the microbial genes reviewed does not give rise to health concerns. We recommend including the above-mentioned items into the premarket safety assessment of genetically modified crops carrying transgenes other than those reviewed in the present study. INTRODUCTION the Organisation for Economic Cooperation and Devel- The cultivation of genetically modified (GM) crops opment (OECD) and International Life Sciences Institute has rapidly increased since their large-scale commercial (ILSI) have initiated this harmonisation. It has recently introduction in 1996. The acreage of GM crops in 2004 culminated into the issuance of FAO/WHO Codex Ali- amounted to 81 millions of hectares worldwide, while the mentarius guidelines for the safety assessment of foods number of nations that adopt GM crop cultivation was derived from GM plants and microorganisms [2]. Cen- also increasing [1]. Before GM crops and other geneti- tral in the harmonised approach is the comparative safety cally modified organisms (GMOs) are allowed to enter the assessment, which entails the comparison of a GMO with market, the law in many nations requires that these organ- a conventional counterpart that has a history of safe use isms and/or derived products be assessed for their safety. [3]. This comparison may include, for example, pheno- To this end, the applicant, which is in most cases a com- typic characteristics (eg, field behaviour) and composi- pany that has developed and produced a GMO, provides tion (eg, macronutrients, micronutrients, antinutrients) ff a dossier to the national authorities, which, among oth- of a GMO and its comparator. Based upon the di erences ers, contains safety data. Whereas national laws and reg- found during the comparison between the GMO and its ulatory procedures may differ among each other, the reg- comparator, it can be decided which further safety tests ulatory safety assessment itself follows an internationally are needed. Issues that are commonly addressed during harmonised approach. International organisations like the safety assessment include the molecular characteri- the United Nations’ Food and Agriculture Organisation sation (eg, introduced genes), the potential for horizon- (FAO) and World Health Organisation (WHO) as well as tal gene transfer, potential allergenicity, potential toxicity, nutritional characteristics, environmental effects, and un- intended effects of the genetic modification (reviewed in [4]). Correspondence and reprint requests to Gijs A. Kleter, RIKILT, Institute of Food Safety, Wageningen University and Research Horizontal gene transfer Center, PO Box 230, 6700AE Wageningen, The Netherlands, Various mechanisms exist for horizontal gene trans- E-mail: [email protected] fer between microorganisms, such as phage transduction, This is an open access article distributed under the Creative conjugation, and transformation by free DNA (eg, [5]). Commons Attribution License which permits unrestricted use, The possible scenario for gene transfer between GM crops distribution, and reproduction in any medium, provided the and microorganisms is, however, limited to transforma- original work is properly cited. tion with free DNA. © 2005 Gijs A. Kleter et al 2005:4 (2005) Health Aspects of Transgene Transfer 327 Anumberofstudiesandreviewshavefocusedon may only be a fraction of what is consumed, DNA is less the transfer of genes from GM plants to soil- and plant- rapidly degraded there. For example, ex vivo and in vivo related microorganisms (eg, [6, 7, 8, 9, 10]). The results of rat models simulating human gut conditions showed that some of these studies indicated that transgenes from GM DNA is rapidly degraded in the upper part of the gastroin- crops are most likely transferred if they contain sufficient testinal tract, but to a lesser degree in the lower part [19]. similarity with the corresponding genes in the recipient Besides the integrity of DNA, the transformability, because homologous recombination is the most probable that is, the likelihood that this DNA will transform bac- mechanism of transfer (eg, [11]). It has, however, recently teria in food or in the gut, should be taken into account. been observed that under conditions of simulated light- In foods, transformation of Escherichia coli by plasmid ning, which might cause electroporation of recipient cells, transfer was proven to occur in all 12 food products in- DNA could be transferred to isolated soil microbes [12]. vestigated [21]. In addition, transfer of DNA to Strepto- Other factors that are important for transformation coccus gordonii was also proven in homogenates of blood with DNA are the natural or induced competence of the sausages by marker rescue experiments [22]. Kharazmi et recipient microorganisms, such as the natural competence al [23] observed the transfer of nptII kanamycin resis- of Campylobacter species. Some microorganisms, such tance marker gene from transgenic potatoes to Bacillus as Salmonella typhimurium,havemismatchrepairsys- subtilis with defective nptII by homologous recombina- tems that form a barrier for recombination between even tion under in vitro conditions. Based upon the observed highly similar sequences (eg, reviewed for Salmonella by frequencies of transfer, these authors calculated the prob- [13]). Some bacteria can develop natural/chemical com- ability of the transfer of the intact nptII gene from con- petence under certain environmental conditions [6]. sumed transgenic potatoes to microbes. Because marker In addition, the transgenes in plants may have been rescue by homologous recombination is the most proba- linked to promoters with optimal activity in the cells ble mechanism for gene transfer, these calculations can be of plants. Sequences promoting expression in eukaryotes considered a “worst-case” scenario in view of other possi- and prokaryotes are generally known to be different. Nev- ble mechanisms of horizontal transfer of transgenes from ertheless, Jacob et al [14] observed that eukaryotic pro- GM crops. moters from, for example, the cauliflower mosaic virus, Potential health effects potato, and tobacco, triggered expression of inserted re- Currently, the focus of the assessment of potential porter genes in five eubacterial species. In addition, Lewin transfer from GMOs is on antibiotic-resistance marker et al [15] observed that random sequences from yeast may genes, as, for example, in the previously mentioned FAO/ exhibit promoter activity in bacteria. WHO Codex Alimentarius guidelines. In a more gen- Jonasetal[16] estimated the potential dietary in- eral sense, antibiotic resistance among microbial hu- take of transgenic DNA present in food. The estimated man pathogens is currently a top priority issue in intake of transgenic DNA from maize, soya, and pota- health care and research. The horizontal gene transfer toes amounted to approximately 0.38 μgperday,assum- of antibiotic-resistance genes between microorganisms ing that only GM crops are consumed. This is about has been important for the development of antibiotic- 0.00006% of the total DNA intake of 0.6gperday. resistant pathogens. Still this is a “worst-case” scenario as DNA is prone to In modern biotechnology, some antibiotic-resistance degradation in food matrices or during food processing marker genes are used for the successful molecular (reviewedin[16]). On the other hand, also the protection cloning in bacteria and plants because they enable growth of DNA against the activity of DNase I in, for instance, on antibiotic-containing media after the genetic modi- fermented sausages has been described [17]. fication process. These marker genes are therefore use- In addition, the integrity of the DNA is countered ful in the development phase, but have no function in by the activity of DNA degrading enzymes released by the final product. An example of an antibiotic-resistance the pancreas and intestinal epithelial cells during its pas- gene that is present in many commercial GM crops is the sage through the gastrointestinal tract. Nevertheless, it has kanamycin-resistance gene nptII encoding the neomycin been shown that DNA can persist in the gastrointestinal phosphotransferase II enzyme. The use of this gene has tract [16, 18, 19] and consequently be
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