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Microbe Hunting W MICROBIOLOGY AND MOLECULAR BIOLOGY REVIEWS, Sept. 2010, p. 363–377 Vol. 74, No. 3 1092-2172/10/$12.00 doi:10.1128/MMBR.00007-10 Copyright © 2010, American Society for Microbiology. All Rights Reserved. Microbe Hunting W. Ian Lipkin* Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York INTRODUCTION .......................................................................................................................................................363 DIVERSITY OF THE MICROBIAL UNIVERSE...................................................................................................364 PROOF OF CAUSATION .........................................................................................................................................364 Possible Causal Relationship................................................................................................................................365 Probable Causal Relationship...............................................................................................................................365 Interventional evidence ......................................................................................................................................366 (i) Challenges ..................................................................................................................................................366 Prophylactic evidence .........................................................................................................................................367 (i) Challenges ..................................................................................................................................................367 Definitive Causal Relationship .............................................................................................................................367 (i) Challenges ..................................................................................................................................................367 ISOLATION OR VISUALIZATION OF INFECTIOUS AGENTS ......................................................................367 COMPLEXITIES OF PATHOGENETIC MECHANISMS MAY CONFOUND DISCOVERY AND IMPLICATION OF MICROBES IN DISEASE ..............................................................................................367 MICROBIAL PROSPECTING .................................................................................................................................368 PATHOGEN DE-DISCOVERY.................................................................................................................................368 Challenges............................................................................................................................................................369 MOLECULAR METHODS FOR PATHOGEN DISCOVERY .............................................................................369 Singleplex Assays ....................................................................................................................................................369 Multiplex Assays .....................................................................................................................................................370 Multiplex PCR Assays............................................................................................................................................370 Microarrays .............................................................................................................................................................370 Unbiased High-Throughput Sequencing..............................................................................................................371 VIGNETTES IN PATHOGEN DISCOVERY..........................................................................................................371 Molecular Characterization of Borna Disease Virus, a Novel Neurotropic Virus ........................................371 West Nile Virus in North America .......................................................................................................................372 Novel Enterovirus in Amyotrophic Lateral Sclerosis ........................................................................................372 Dandenong Virus, a New Lymphocytic Choriomeningitis Virus......................................................................372 Measles-Mumps-Rubella Vaccine and Autism ...................................................................................................373 Streptococci and Novel H1N1 Pathogenicity.......................................................................................................373 FUTURE PERSPECTIVES........................................................................................................................................374 ACKNOWLEDGMENTS ...........................................................................................................................................374 REFERENCES ............................................................................................................................................................374 INTRODUCTION In 1967, U.S. Surgeon General William Stewart was re- ported to have said that given advances in antibiotics and In 1926, Paul de Kruif published Microbe Hunters (40a), a vaccines, it was time to “close the book” on infectious dis- book that captured the imagination of generations of bud- eases so as to free resources to focus on chronic illness (22). ding microbiologists. Subsequent contributions, including Microbe Hunters—Then and Now, by Koprowski and Old- There is no formal annotation of the remark, and Stewart stone (68a), have summarized advances and disease over- himself disavowed any knowledge of making it. Nonetheless, views possible to that time. However, recent increases in the the fact that this apocryphal quote survives suggests that at rate of speed of pathogen discoveries call for us to take a least some held similar views at the time. The fallacy of such deep breath and see where we are. This paper summarizes misplaced optimism was amply illustrated in the years that and compares methods now in use and suggests possible followed, as a host of new plagues were discovered, for exam- directions in which we might travel over the next few years, ple, HIV/AIDS and bovine spongiform encephalopathy, as providing rationales and examples of discoveries. It is well as old ones in new clothing, such as antibiotic-resistant weighted more toward viruses than other microbes because staphylococci, various mycobacteria, and Escherichia coli this reflects the experience of the author; nonetheless, I O157:H7. Perhaps more intriguing than these discoveries has have tried to emphasize issues generic to the field. been the recognition that the notion of infectious diseases as always being acute is too narrow. Microbes have been linked to a wide range of chronic illnesses, including ulcers, cancer, * Mailing address: Center for Infection and Immunity, Mailman cardiovascular disease, and mental illness. Thus, rather than School of Public Health, Columbia University, 722 West 168th Street, 17th Floor, New York, NY 10032. Phone: (212) 342-9033. Fax: (212) closing the book on infectious diseases, new chapters are being 342-9044. E-mail: [email protected]. written. 363 364 LIPKIN MICROBIOL.MOL.BIOL.REV. DIVERSITY OF THE MICROBIAL UNIVERSE versity are staggering. In addition to serving as potential res- ervoirs for the emergence of novel pathogens, these viruses Can we actually “know” the universe? My God, it’s hard may serve a critical function in global as well as marine eco- enough finding your way around in Chinatown. systems by controlling prokaryote multiplication (124). —Woody Allen The introduction of cultivation-independent methods for PROOF OF CAUSATION microbial discovery and surveillance has dramatically altered our view of the breadth and diversity of the microbial world. Finding an organism in association with disease is only the Not only can we now find and characterize disease agents for first step in establishing a causal relationship (Fig. 2). Pasteur, which we have no culture system, we can also more rapidly Koch, and Loeffler proposed precise criteria that define a caus- survey ourselves and the larger biosphere. These advances ative relationship between agent and disease. In what are now have enabled extraordinary revelations. One example is the known as Koch’s postulates, these criteria require that an agent extent to which humans represent microbial vessels. Whereas be present in every case of the disease, be specific for that the number of cells of the human body has been estimated to disease, and be propagated in culture and proven capable of be 1014, our bacterial passengers on internal and external sur- replicating the original disease upon inoculation into a naïve faces number at least 1015 (115). Furthermore, up to 10% of host (68). Rivers modified these criteria for specific application our genomes comprise retroviral sequences (52). 16S rRNA to viruses (110), focusing on the presence of neutralizing an- gene analyses of the oropharynx (1), esophagus (105), stomach tibodies as evidence of specificity. Fredericks and Relman (11), intestine and colon (43), vagina (94), and skin (49) indi- adapted them to reflect the introduction of PCR, requiring the cate differences in human
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