Microbiological material exchanges among scientists

Research in Microbiology 161 (2010) 446e452 www.elsevier.com/locate/resmic

Microbiological material exchanges among scientists James T. Staley a, Kelly FitzGerald b, John A. Fuerst c, Lenie Dijkshoorn d,* a

Department of Microbiology, University of Washington 357242, Seattle, WA 98195, USA Technology Transfer Office, University of Washington 357242, Seattle, WA 98195, USA c School of Molecular and Microbial Sciences, University of Queensland, St. Lucia, Queensland 4072, Australia d Department of Infectious Diseases C5-P, Leiden University Medical Center, Albinusdreef 2, P.O. Box 9600, 2300 RC Leiden, Netherlands b

Received 23 May 2010; accepted 31 May 2010 Available online 15 June 2010

Abstract Traditionally, biologists exchange scientific materials with other scientists to enable the independent confirmation of their research. For example, in microbiology, cultures of bacteria and other microorganisms and viruses are commonly sent to other laboratories upon request. Apart from this, it is a requirement of the International Code of Nomenclature for Prokaryotes, that culture type strains of a novel bacterial species be deposited in ‘at least two different publically accessible service collections in different countries from which the subcultures must be available’ to ensure their availability to all other scientists who may wish to study them. However, special challenges have recently been encountered in transporting such strains in order to meet such needs. This paper discusses the use of material exchanges and the challenges in this field. Ó 2010 Elsevier Masson SAS. All rights reserved. Keywords: Microbiological material exchange; Material transfer agreements; Microbial commons

1. Introduction One of the great traditions of science is the free exchange of materials among scientists. Biological materials such as cultures of bacteria, purified enzymes or cloned genes are freely shared with others in the field primarily to validate the claims of published research. Sharing between laboratories is also important to allow for collaborative studies using techniques that are not available to each individual laboratory. These common practices have spurred scientific inquiry and furthered research. Material exchange agreements are a more recent phenomenon arising in large part from the desire to attain a fair and appropriate allocation of proprietary rights arising from collaborative research or from the commercialization of biological products. This paper provides examples of exchange of materials, or the occasional lack of them, ownership issues and * Corresponding author. E-mail addresses: [email protected] (J.T. Staley), kafg@ u.washington.edu (K. FitzGerald), [email protected] (J.A. Fuerst), [email protected] (L. Dijkshoorn). 0923-2508/$ - see front matter Ó 2010 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.resmic.2010.05.011

constraints which arise in the free exchange of materials due to safety regulations.

2. The transfer of biological materials in the scientific community 2.1. Reasons for exchanging materials There are numerous scientific reasons for exchanging biological materials among scientists and institutes. In many cases, these exchanges provide added scientific value. One example is a personal experience of one us (JTS) in the late 1960s regarding some novel bacteria from aquatic habitats (Fig. 1; Staley, 1968). The organisms had multiple cellular appendages, named prosthecae that extended from the cells. These findings attracted the interest of Rogier Stanier, who received the cultures for independent substantiation and confirmation of the findings. It so happened that, at that time, Stanier’s wife, Germain Cohen-Bazire, was collaborating with Norbert Pfennig on the gas vesicles of photosynthetic bacteria

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Fig. 1. Several cells of the multiple-appendaged prosthecate bacterium, Ancalomicrobium adetum, as observed by scanning electron microscopy. Pores in nucleopore filter are 0.2 mm in diameter.

(Pfennig, 1967). Gas vesicles are proteineaceous organelles that are produced by certain aquatic bacteria as organelles of buoyancy. They enable the cells to rise or descend in the water columns of lakes and in marine environments such as sea ice. When Stanier and Cohen-Bazire examined Staley’s cultures, they discovered that some of the bacteria had gas vesicles which had been noticed by Staley but were not recognized as such because they were unknown in any bacteria aside from the cyanobacteria at that time (Fig. 2). This illustrates that exchanging scientific materials can be extremely beneficial to the provider as well as the recipient. Another illustration of the importance of material transfers comes from the famous postulates of Robert Koch. In Koch’s postulates, several steps are laid out that are necessary to fulfill in order to “prove” that a specific microorganism is the causative agent of a disease. These steps entail having a pure culture that can be sent to another laboratory to confirm the results indicating

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that a specific organism is the causative agent of a specific infectious disease. These same postulates have been extended to ecological studies in which a claim has been made that a specific microorganism, or consortium of organisms, is the causative agent of a specific process such as nitrogen fixation. For this reason, it is incumbent upon the scientist who reports the new finding in a scientific paper to retain the culture or consortium, even though it has not been named. Only by doing this can the work of the scientist be substantiated by another who requests the culture or consortium for verification and further studies. In taxonomy, the exchange of bacterial strains is important for two reasons. First, the description of novel species may require collaboration between researchers to characterize the strains of this species according to current standards. These standards include a polyphasic approach (Vandamme et al., 1996) comprising a combination of methods including DNAeDNA hybridization, sequence analysis of particular genes, chemotaxonomic methods and phenotypic characterization (Moore et al., 2010). Usually, not all these methods are commonly used in laboratories (except for a few taxonomic centers of excellence) when studying the taxonomy of a particular group of organisms. This can be overcome by collaboration between research groups with different expertise to characterize the concerned organisms according to recommended guidelines. Secondly, for description of a novel species, it is important that multiple strains of this species be compared to each other to assess the diversity of this species, and collaboration among microbiologists to bring such sets together is important. Unfortunately, numerous recent descriptions of novel species in the International Journal of Systematic and Evolutionary Microbiology (IJSEM) are based on the description of one strain only. This has the disadvantage that phenotypic and genotypic variation within the species cannot be determined, and unambiguous assignment of new isolates to the species (¼identification) may become extremely difficult, or even impossible. This development has been criticized by e.g. Christensen et al. (2001), who proposed the use of a (theoretical) minimum of five strains for new species descriptions. However, other taxonomists argue that it may be difficult to isolate multiple strains that are representatives of novel orders, classes and phyla from which none or few strains currently exist in culture. In these situations, a single rare strain should be sufficient in that it will enable scientists to learn much about the features of the unusual taxonomic group. From a microbial commons point of view it would be advantageous to have a ‘public portal’ of candidate strains for novel species to bring together multiple strains of the same species, thus allowing for description of novel species of multiple strains. To what extent taxonomists will be able to deal with the rapid increase in novel species of one strain only is a challenging question for the International Committee on the Systematics of Prokaryotes (ICSP). 2.2. Ignorance of requests or refusals to provide materials

Fig. 2. A single cell of Ancalomicrobium adetum showing its gas vesicles, appearing as many small relatively electron-transparent regions in the cytoplasm, as observed by transmission electron microscopy (TEM) of a negatively stained cell.

It may happen that a request from a laboratory to provide published material is not honored. Sometimes, there is no reply at all to the request. It may also happen that the reply is

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that the material is no longer available or accessible. For instance, clinicians who participate in microbiological studies may state that the actual laboratory work was done by someone else and that he/she cannot provide it. Current stringent regulations on the shipment of microorganisms to other laboratories also do not contribute to the free exchange of microbiological materials, since compliance is an expensive and laborious activity. Another reason for hesitating to exchange materials might be that the organism is already under investigation for the same type of research as the requesting scientist has in mind. In the latter case, some form of collaboration might be a good compromise. In competitive research, the use of a material transfer agreement (MTA) (see below) to safeguard the rights of the providing institute can be important to avoid conflicts of interest. 3. Requirement for deposition of pure cultures in culture collections Rules of the International Code of Nomenclature for Bacteria (Sneath, 1992; Tindall et al., 2008) require that anyone who names a new species of Bacteria or Archaea must deposit a strain of the new species in at least two publically accessible service collections in different countries for which the subculture must be available (Tindall et al., 2008; see also e.g. http://www.wfcc.info/ for World Federation of Culture Collection (WFCC) or http://www.eccosite.org/ for European Culture Collections Organization (ECCO)). These originally named and deposited strains are referred to as type strains of the species, and the culture collections make them available to all scientists who wish to include them in comparative biodiversity/taxonomic studies. These culture collections (Biological Resource Centers or BRCs, according to the OECD; see also (Janssens et al. (2010), this issue)) charge a modest sum to those who wish to receive subcultures of these strains in order to cover growth, maintenance and shipping costs. Culture collections may currently request that the scientist who deposits the strain sign a MTA. This practice will be discussed later in a separate section. Apart from the depositing of type strains, it is important that strains of microbial interest, including those described in publications for a number of e.g. clinical or biotechnologically important features, be deposited at microbial resource centers. Several microbial societies, including the ASM and FEMS, have stated in the instructions to authors of papers submitted to their journals that they “expect authors to deposit important strains in publicly accessible culture collections and to refer to the collections and strain numbers in the text or at least expect the author to make important material available”. It is not clear to what extent there is compliance with this rule and what the consequences are in case of non-compliance. For a microbial commons it is important that microbial societies, scientific journals and institutions support and adhere to such recommendations. The availability of, and the need for, biological material in particular microorganisms was recently acknowledged in the literature (e.g., Beattie and Ehrlich, 2010).

4. Difficulties in exchange and shipment Cultures of species with no or low individual and community risk (Risk Group 1, World Health Organization classification, WHO, 2004) like, e.g. Bacillus subtilis, that are easy to isolate and maintain can be easily shipped to another laboratory. However, shipment of microorganisms can be difficult for two reasons. One is that some bacteria are difficult to grow and may not survive shipment or else require special precautions to safeguard their survival (Table 1). One of the authors (JTS) experienced difficulties with the shipment of several of these organisms. One example was Cycloclasticus pugetii, a marine bacterium that degrades polycyclic aromatic hydrocarbon (PAH) compounds found in crude oil and therefore in oil spills, but which is difficult to isolate in pure culture and does not grow easily in the lab (Dyksterhouse et al., 1995). Also, some sea ice bacteria, including the genus Polaribacter (Gosink et al., 1998), are extreme psychrophiles that die when left at room temperature overnight. Therefore, they must be shipped frozen or on blue ice by overnight air express. This is expensive and there is no guarantee that the shipments will arrive at a remote destination in due time to survive the shipping process. Another organism that is difficult to grow is the tubulin-containing bacterium, Prosthecobacter dejongeii (Jenkins et al., 2002; Hedlund et al., 1997). This species as well as others in the genus grow very slowly to very low cell densities. It forms small colonies on plates, but by the time the colonies appear the cells have begun to die. Thus, it is difficult to work with these strains as well as to ship them to other laboratories. Shipment of pathogenic bacteria requires special handling. Not too long ago, it was possible for almost anyone, regardless of scientific background, to obtain a culture, even of pathogenic bacteria, from culture collections. In some cases, this led to the shipment of human pathogenic strains to individuals with nefarious ideas. That particular loophole has now been closed, thanks in part to the anthrax scare that followed the 9/11 massacre of the World Trade Center in New York City. At present, only qualified recipients can receive pathogenic bacterial cultures. Thus, international shipment of bacterial strains that are potentially pathogenic to humans and animals has become an expensive and time-consuming affair, in particular for shipments to and from the USA. Further to the shipping of pathogenic organisms, there are special challenges for shipping cultures to some countries. For example, Australia has strict quarantine requirements for receiving bacterial cultures even when they are not pathogenic. Quarantine import permits must be carefully completed, a signed “manufacturer’s declaration” must be included with the parcel describing how the cultures were prepared and their identity, and arrangements must be made to coordinate shipping with their arrival in Australia. This can be timeconsuming and pose special difficulties if the cultures must be refrigerated or frozen after growth while waiting for permits to be issued. Altogether, application and import permit processes can take several months, necessitating a “biosecurity” office for examining applications even when strains are not known to be pathogenic to animals or plants.

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Table 1 Special issues with exchanges of bacterial culture. Feature and example of culture

Degree of difficulty/challenge

Expense

Easy to grow and ship (example: Bacillus subtilis) Difficult to grow, easy to ship (example: Cycloclasticus pugetii) Easy to grow, difficult to maintain (example: psychrophilic sea ice bacteria, e.g. Polaribacter irgensii) Difficult to grow and maintain (example: Prosthecobacter species) (Potentially) pathogenic organisms (example Risk groups 2e4 of WHO classification)

Simple for sender and recipient

Modest

Difficult for recipient

Modest

Recipient must receive refrigerated or frozen culture quickly, as cells die at room temperature Culture dies soon after growth

Expensive

Expensive

Difficult

Very expensive

5. MTAs in the scientific community Traditionally, MTAs have not been used by scientists when exchanging materials for scientific purposes. As mentioned previously, the primary goal of exchanging cultures is to permit verification of scientific studies by independent laboratories. This process of free exchange continues today as a hallmark of scientific research. This principle of free exchange extends to bacterial cultures as well, keeping in mind that pathogenic bacteria and customs issues may pose some challenges. However, increasingly there is a movement toward use of MTAs in microbiology. This practice has arisen primarily with commercial enterprises and culture collections. Furthermore, it is an increasingly common practice for research institutions to use MTAs, although some microbiologists have argued that MTAs actually threaten the field of bacterial taxonomy because of their interference with the open flow of cultures (Tru¨per and Tindall, 2005). Most MTAs aim to preserve the open sharing of cultures by using special provisions which permit further exchange of cultures between culture collections and collaborating scientists. However, there is also an increasing trend toward the use of restrictive MTAs by some collections both in developed and developing nations (Dedeurwaerdere, 2010). Despite these negative aspects of MTAs on the generally accepted exchange policy between scientists of biological material, MTAs are also beneficial, in particular regarding the safeguard of quality and authenticity of biological material. Indeed, BRCs (or culture collections) are increasingly setting up a TQM (total quality management system; e.g. ISO denomination) in order to check the purity and authenticity of the reference material (¼the type strains) of holdings that they distribute. MTAs should prevent these reference cultures from being distributed via uncontrolled networks amongst scientists, thus ensuring that non-authenticated material will not be included in studies or tests.

commercial or scientific value, is an important activity in many natural environments. This activity and its spin-off also raise the question of the ownership of newly discovered species (Table 2). Certainly, the scientist who has discovered a novel organism is a stakeholder in the process. Table 3 itemizes steps typically taken by a scientist who endeavors to isolate and describe a new species of Bacteria or Archaea. The scientist must first isolate the organism in pure culture. This is not always easy because it is estimated that less than 1% of the total bacteria in nature grow at present on typical laboratory media or under typical laboratory conditions; therefore, the vast majority of them have not been isolated in pure culture (Mocali and Benedetti, 2010; Staley and Konopka, 1985). The work entailed by the scientist who isolates and describes a new species requires several months and therefore represents a considerable input of resources and time. For these reasons, the scientist surely must be considered a stakeholder in any commercialization of the organism. A significant example relating to this issue of ownership can be found in the literature. The thermophilic bacterial species Thermus aquaticus was isolated and named by Thomas Brock’s laboratory. The species was isolated from a hot spring in Yellowstone National Park. Kary Mullis, who obtained the strain from the ATCC, used DNA polymerase (Taq polymerase) from this bacterium in his patent with Cetus Corporation (Berkeley, CA, USA) for the polymerase chain reaction (PCR). He received the 1993 Nobel Prize in Medicine for this invention. Table 2 Possible priority list of claiming rights for value of parties involved in description of novel species. Party

Contribution to discovery

Scientist Source of financial support

Discovers, isolates, describes and deposits Employera, governmental or private funding to support research Source of strain (Rio de Janeiro agreement) Curator: maintains culture and distributes it Provide description and validation information on bacterial species

6. Ownership issues

Property owner? Culture collection IJSEMb; Bergey’s Manualc

Currently, there is increasing awareness that nature harbors a multitude of yet undescribed species including prokaryotes, plants and animals, many of which are scientifically or commercially valuable. Thus, it is not surprising that “bioprospecting”, i.e. the search for biological specimens that have

a University or other employer typically claims ownership rights that may be shared with scientist. b International Journal of Systematic and Evolutionary Microbiology is where validation of bacterial species occurs. c Bergey’s Manual of Systematic Bacteriology contains a description of all bacterial species.

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Table 3 Work entailed for microbiologist who describes a novel species. 1. Engineering the isolation of a pure culture. Development of enrichment conditions that select for organism of interest. Isolation of pure culture of desired organism (includes selection of environmental source, designing conditions for growth, media preparation, incubation, isolation maintenance and preservation). 2. Characterization of the novel species (or consortium). Performing a large variety of phenotypic tests (growth substrates, temperature range, oxidase, catalase and other enzyme tests, vitamin requirements, etc, depending on the needs for comparison to closely related bacteria or archaea). Analysis of 16S rRNA gene sequence and phylogeny. Determination of mol% G þ C content. DNA e DNA hybridization analyses. 3. Depositing of the strain in two different culture collections. 4. Depositing of 16S rRNA gene sequence and/or sequences of other housekeeping genes in GenBank. 5. Description of novel strain in a publication, ultimately validated in the International Journal of Systematic and Evolutionary Microbiology.

The PCR technique has been very successful commercially. This raises the question of who should receive the benefits from its commercial success. In this particular instance, the only recipient of the royalties is the owner of the patent held by the company. The scientist who originally isolated the organism receives no returns, nor does the US National Park Service which operates Yellowstone National Park, nor does the property owner or the ATCC, which has preserved the biological material. Yet it can be argued that they have all contributed labor, time and intellectual resources. In response to this particular and rare example of successful commercialization of a product from a bacterium, the US National Park Service now claims real property rights to the organisms found in the National Parks. The ATCC has an agreement with the National Park Service for these rights (Perrone and Soriano, 2005). The US National Institutes of Health has issued guidelines that describe the rights of the scientists involved. Consistent with these guidelines, the scientist who originally patented the PCR process and his company received all rights to use of Taq polymerase. In contrast, the scientist who isolated, described and named the organism has no “reach-through” rights because the original work did not involve the organism’s DNA polymerase. However, the scientist who described the organism could request reimbursement for isolating, describing and depositing the strain. Because of the important role played by the scientist who discovered, named and deposited the organism, one can support the proposal that Jerome Reichman and co-authors (Rai et al., 2009; Reichman, 2000; Reichman et al., unpublished) have made to automatically allow reachthrough rights with modest potential royalties of 2e5% for the scientist in conjunction with his/her employer (and/or the upstream depositor) as part of routine MTAs. This agreement would apply to all material transfers, but the royalties would only be triggered in the case of commercial applications without any need for cumbersome negotiations. It should be mentioned, however, that the major mission of BRCs is

preservation and distribution of biological material that reflects biodiversity for fundamental scientific reasons and hence, substantial support by national and international funding bodies will remain a prerequisite for reaching that goal. Typically a university scientist and/or laboratory unit who isolates and describes microorganisms with commercial potential shares the benefits of commercial use with the university who employs him/her, based on internal rules of the university which holds rights to the resources (except if there is a special arrangement with an external funding agency). Therefore, so-called “technology transfer offices” have been set up at universities in the US and elsewhere to facilitate protection of the scientist’s rights in terms of eventual patent deposits, funding agencies and broad dissemination of scientific results and biological material. MTAs may be part of this approach. The question of the rights of real property owners has also arisen, with respect to the 1992 Rio de Janeiro Convention on Biological Diversity (Tate, 2004) which reaffirmed the sovereign rights of states over their resources. Among the issues discussed at the convention was “access to and fair and equitable benefit sharing of uses of genetic material.” Although the USA did not sign this Convention, some US pharmaceutical companies have contracted with third-world countries to obtain and use their genetic resources. For example, Merck contracted with INBio in Costa Rica for access to their plants, animals and microbes as sources of potentially useful biotechnological resources such as antibiotics (Tamayo et al., 2004; Svarstad, 2004). Other companies such as Diversa have made similar arrangements with the US National Park Service (Doremus, 2004). However, except for these and other isolated cases, the majority of the exchanges are done without explicit contracts containing benefit-sharing clauses, and as a result the issue of international exchanges for commercial uses remains a very contentious issue (Safrin, 2004). 7. MTAs for patented materials A university’s primary goals are to further knowledge and to disseminate that knowledge to the public. The first goal requires funding in addition to solid science, and the second can happen in several ways. The primary means of transferring university knowledge to the public is through the training of students and the publishing of scientific peer-reviewed journal articles. Historically, this was also the only means of doing this. In the United States, in 1980, the Bayh-Dole act was signed giving universities the right to retain ownership of intellectual property arising from federally funded research. This act has had a profound effect on the way intellectual property is protected and transferred from US academic institutions to the public. Primarily, the result has been an increase in patent filings by US universities, from less than 250 patents per year to over 11,000 in 2004 (AUTM, 2008). With this new emphasis on protecting intellectual property, universities have had to

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develop technology transfer offices to manage their burgeoning patent portfolios. In addition to managing the patents, these offices are responsible for licensing the patents to commercial entities and then ensuring that product development is diligently pursued. With all of this investment of resources in patents, MTAs have become increasingly important to ensure that universities are not violating the patents of other entities when they send out strains, and that appropriate conditions are set for the use of the materials. This practice is necessary to place exchanges on a sound legal basis when involving patented materials, and can contain clauses that favor further use for research, such as a non-exclusive noncommercial use license or access to research materials within a public/private partnership (cf. Fig. 3). It is questionable, however, whether this development in bureaucracy is productive and in compliance with a true microbial commons, especially for the bulk of research materials that are exchanged with no patent claims attached and/or with still unknown commercial potential. Data on patent statistics (Compendium of Patent Statistics, OECD, 2008) show that 5e10% of patents both in Europe and in the US concern biotechnology applications, a fraction of which involve the use of microorganisms. It is important to mention here that, for those patents, the Budapest treaty (http://www.wipo.int/ treaties/en/registration/budapest/trtdocs_wo002.html) requests deposit in an IDA (International Depositary Authority) where the organism is preserved for 30 years (with possible extension of another five years) and at which the organism is available and regularly controlled for viability. 8. Closing remarks Science and technology thrive on the free exchange of ideas and scientific material such as microbial cultures. Both private companies and universities agree on this. Scientists belong to

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several communities, and they have obligations to each of them. They belong to their research institution, whether it is a public university or a private company. This relationship is governed by their employment agreement. They are also citizens operating within the regulatory framework governing import and export of biological material. The exchange of scientific materials such as bacterial cultures may also involve challenges due to increasing requirements placed by regulatory agencies as well as those due to purely technical problems. Increased communication and understanding of the needs of professional scientific activity and of regulatory agencies on the part of both regulatory agencies and the scientific community may be necessary for all parties to facilitate efficient scientific productivity and its applications. In addition, scientists belong to an informal community of fellow scientists with whom they have both implicitly and explicitly agreed to share their discoveries and, on occasion, discovery-related research materials. All scientists in the community need to understand the necessity for generous exchange of materials to facilitate the advancement of their science, allowing for the constraints set by increasing regulation of such transfer by both government and research organizations. Finally, in the case of collaboration, scientists have obligations to their collaborators. Because of this complex network of obligations, written agreements are often necessary before institutions are willing to work together. When scientists wish to exchange materials for scientific purposes and for purposes mandatory within taxonomic rules, as well as applying MTAs, historically established principles of free exchange should also be taken seriously, especially by legislators and regulators. In a 21st century biotechnological civilization, the latter may be pivotal for facilitating such scientific activity and discovery. Acknowledgements The authors wish to acknowledge the assistance of Cheryl Jenkins, who helped develop the collection of strains, Benjamin Yee, who prepared shipment of strains to Dow AgroSciences and Australia and is further characterizing the strains, Don Hahn and Clegg Waldron of Dow AgroSciences, with whom the authors collaborated, and Carol Rhodes of the UW Office of Sponsored Programs. In addition, the authors appreciate the financial assistance of Dow AgroSciences. References

Fig. 3. Diagram showing the outline of the research collaboration agreement between the University of Washington in the US (UW), the University of Queensland (UQ) in Australia and Dow AgroSciences (DOW).

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