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Workshop Overview1 THE SCIENCE AND APPLICATIONS OF MICROBIAL GENOMICS: PREDICTING, DETECTING, AND TRACKING NOVELTY IN THE MICROBIAL WORLD Over the past several decades, new scientific tools and approaches for de- tecting microbial species have dramatically enhanced our appreciation of the diversity and abundance of the microbiota and its dynamic interactions with the environments within which these microorganisms reside. The first bacterial genome2 was sequenced in 1995 and took more than 13 months of work to com- plete. Today (2012), a microorganism’s entire genome can be sequenced in a few days. Much as our view of the cosmos was forever altered in the 17th century with the invention of the telescope (Nee, 2004), these genomic technologies, and the observations derived from them, have fundamentally transformed our apprecia- tion of the microbial world around us. Nucleic acid sequencing technologies now provide access to the previously “unculturable”—and thus, undetected—microorganisms that comprise the ma- jority of microbial life. Rapid and inexpensive sequencing platforms make it 1  The planning committee’s role was limited to planning the workshop, and the workshop summary has been prepared by the workshop rapporteurs (with the assistance of Pamela Bertelson, Rebekah Hutton, and Katherine McClure) as a factual summary of what occurred at the workshop. Statements, recommendations, and opinions expressed are those of individual presenters and participants, and are not necessarily endorsed or verified by the Institute of Medicine, and they should not be construed as reflecting any group consensus. 2  For the purposes of this summary, the genome is defined as the complete set of genetic informa- tion in an organism. In bacteria, this includes the chromosome(s) and plasmids (extrachromosomal DNA molecules that can replicate autonomously within a bacterial cell) (Pallen and Wren, 2007). 1

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2 THE SCIENCE AND APPLICATIONS OF MICROBIAL GENOMICS commonplace to sort through the genomes of dozens of strains of a single mi- crobial species or to conduct “metagenomic” analyses of vast communities of the microbiota from a wide variety of environments. These technical advancements and concurrent investments in the fields of microbial ecology, evolution, foren- sics, and epidemiology have transformed our ability to use genomic sequence information to explore the origins, evolution, and catalysts associated with his- torical, emergent, and reemergent disease outbreaks. The ability to “read” the nucleic acid sequence of microbial genomes has provided important insights into this previously hidden, unculturable world by revealing the vast diversity and complexity of microbial life around us, and their myriad interactions with their abiotic and biotic environmental niches. Recent examples of the use of “whole genome” sequencing to investigate outbreaks of emerging, reemerging, and novel infectious diseases illustrate the potential of these methods for enhancing disease surveillance, detection, and response efforts. Using slight sequence differences between isolates to discrimi- nate between closely related strains, investigators have tracked the evolution of isolates in a disease outbreak, traced person-to-person transmission of a com- municable disease, and identified point sources of disease outbreaks. When ge- nomic information about related strains or past disease outbreaks is available, the genome sequence of outbreak strains has proved useful in identifying factors that may contribute to the emergence, virulence, or spread of pathogens, as well as in speeding diagnostic tool development. In a recent development, fast genome sequencing was used to halt the spread of a methicillin-resistant Staphylococcus aureus (MRSA) infection in a neonatal ward in a hospital in Cambridge, United Kingdom (Harris et al., 2012) Statement of Task On June 12 and 13, 2012, the Institute of Medicine’s (IOM’s) Forum on Microbial Threats convened a public workshop in Washington, DC, to discuss the scientific tools and approaches being used for detecting and characterizing mi- crobial species, and the roles of microbial genomics and metagenomics to better understand the culturable and unculturable microbial world around us. 3 Through invited presentations and discussions, participants examined the use of microbial genomics to explore the diversity, evolution, and adaptation of microorganisms in 3  A public workshop will be held to explore new scientific tools and methods for detecting and characterizing microbial species and for understanding the origins, nature, and spread of emerging, reemerging, and novel infectious diseases of humans, plants, domestic animals, and wildlife. Topics to be discussed may include microbial diversity, evolution, and adaptation; microbial genomic, epi- demiology, and forensic tools and technologies; infectious disease detection and diagnostic platforms in clinical medicine, veterinary medicine, plant pathology, and wildlife epidemiology; development of microbial genomic and proteomic databases; and strategies for predicting, mitigating, and responding to emerging infectious diseases.

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WORKSHOP OVERVIEW 3 a wide variety of environments; the molecular mechanisms of disease emergence and epidemiology; and the ways that genomic technologies are being applied to disease outbreak trace back and microbial surveillance. Points that were em- phasized by many participants included the need to develop robust standardized sampling protocols, the importance of having the appropriate metadata (e.g., the sequencing platform used, sampling information, culture conditions), data analysis and data management challenges, and information sharing in real time. Organization of the Workshop Summary This workshop summary was prepared by the rapporteurs for the Forum’s members and includes a collection of individually authored papers and com- mentary. Sections of the workshop summary not specifically attributed to an individual reflect the views of the rapporteurs and not those of the members of the Forum on Microbial Threats, its sponsors, or the IOM. The contents of the unattributed sections of this summary report provide a context for the reader to appreciate the presentations and discussions that occurred over the 2 days of this workshop. The summary is organized into sections as a topic-by-topic description of the presentations and discussions that took place at the workshop. Its purpose is to present information from relevant experience, to delineate a range of pivotal issues and their respective challenges, and to offer differing perspectives on the topic as discussed and described by the workshop participants. Manuscripts and reprinted articles submitted by some but not all of the workshop’s participants may be found, in alphabetical order, in Appendix A. Although this workshop summary provides a distillation of the individual presentations, it also reflects an important aspect of the Forum’s philosophy. The workshop functions as a dialogue among representatives from different sectors and disciplines and allows them to present their views about which areas, in their opinion, merit further study. This report only summarizes the statements of participants over the course of the workshop. This summary is not intended to be an exhaustive exploration of the subject matter, nor does it represent the findings, conclusions, or recommendations of a consensus committee process. GLIMPSES OF THE MICROBIAL WORLD Microbiologists investigate a largely hidden world, laboring to understand the structure and function of organisms that are essentially invisible to the naked eye. Critical methodological advances—from microscopy through metagenomics— have made the staggering diversity of the microbial worlds on this planet easier to study and have brought them into focus (Table WO-1). Over the past several centuries, these approaches have provided ever-expanding views of the extraor- dinary organismal, metabolic, and environmental diversity of microorganisms.

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4 THE SCIENCE AND APPLICATIONS OF MICROBIAL GENOMICS TABLE WO-1  Some Major Methods for Studying Individual Microbes Found in the Environment Method Summary Comments Microscopy Microbial phenotypes can be studied The appearance of microbes is not by making them more visible. In a reliable indicator of what type of conjunction with other methods, microbe one is looking at. such as staining, microscopy can also be used to count taxa and make inferences about biological processes. Culturing Single cells of a particular microbial This is the best way to learn about type are grown in isolation from other the biology of a particular organism. organisms. This can be done in liquid However, many microbes are uncultured or solid growth media. (i.e., have never been grown in the lab in isolation from other organisms) and may be unculturable (i.e., may not be able to grow without other organisms). rRNA-PCR The key aspects of this method are the This method revolutionized microbiology following: (a) all cell-based organisms in the 1980s by allowing the types and possess the same rRNA genes (albeit numbers of microbes present in a sample with different underlying sequences); to be rapidly characterized. However, (b) PCR is used to make billions of there are some biases in the process that copies of basically each and every make it not perfect for all aspects of rRNA gene present in a sample; this typing and counting. amplifies the rRNA signal relative to the noise of thousands of other genes present in each organism’s DNA; (c) sequencing and phylogenetic analysis places rRNA genes on the rRNA tree of life; the position on the tree is used to infer what type of organism (a.k.a. phylotype) the gene came from; and (d) the numbers of each microbe type are estimated from the number of times the same rRNA gene is seen. Shotgun The DNA from an organism is This has now been applied to over 1,000 genome isolated and broken into small microbes, as well as some multicellular sequencing fragments, and then portions of species, and has provided a much of cultured these fragments are sequenced, usually deeper understanding of the biology species with the aid of sequencing machines. and evolution of life. One limitation is The fragments are then assembled into that each genome sequence is usually a larger pieces by looking for overlaps snapshot of one or a few individuals. in the sequence each possesses. The complete genome can be determined by filling in gaps between the larger pieces.

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WORKSHOP OVERVIEW 5 TABLE WO-1  Continued Method Summary Comments Metagenomics DNA is directly isolated from an This method allows one to sample the environmental sample and then genomes of microbes without culturing sequenced. One approach to doing this them. It can be used both for typing and is to select particular pieces of interest counting taxa and for making predictions (e.g., those containing interesting of their biological functions. rRNA genes) and sequence them. An alternative is ESS, which is shotgun genome sequencing as described above, but applied to an environmental sample with multiple organisms, rather than to a single cultured organism. SOURCE: Eisen (2007). There are three recognized domains of life: the Archaea, the bacteria, and the eukarya. Microorganisms are now recognized as the primary source of diversity for life on Earth and its inhabitants (Figure WO-1). Even more astonishing, per- haps, is what still remains to be discovered about the microbiota on this planet. As Fraser et al. (2000) have observed, “The genetic, metabolic and physiological diversity of microbial species is far greater than that found in plants and animals. The diversity of the microbial world is largely unknown, with less than one-half of 1% of the estimated 2–3 billion microbial species identified [emphasis added].” Moreover, while there are well over 10 million species of “known” bacteria only a few thousand have been formally described (Eisen, 2007). With the advent of genomic technologies, we are entering a new era of scientific discovery that holds great promise for revealing the breadth of diversity and depth of complexity inherent to the microbial world. From Animalcules to Germs Until just over 300 years ago, the microscopic world that we share the planet with was largely unseen and unknown. In the 17th century, Antonie van Leeuwenhoek provided the first detailed glimpses of the “animalcules” in the mi- crobial world when he developed viewing techniques and magnifying lenses with sufficient power to see microorganisms. Van Leeuwenhoek obtained these organ- isms, as illustrated in Figure WO-2, from a variety of environmental sources, ranging from rain and pond water to plaque biofilms scraped from teeth. Their simple morphologies prevented the precise identification and classification of these organisms, but through detailed descriptions and illustrations in his letters to the Royal Society of England, van Leeuwenhoek brought the invisible world of microscopic life forms to the attention of scientists (Handlesman, 2004).

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6 THE SCIENCE AND APPLICATIONS OF MICROBIAL GENOMICS FIGURE WO-1  Universal tree of life based on a comparison of nucleic acid (RNA) sequences found in all cellular life (small subunit ribosomal RNA). “A sobering aspect of large-scale phylogenetic trees such as that shown in Figure WO-1 is the graphical realiza- tion that most of our legacy in biological science, historically based on large organisms, has focused on a narrow slice of biological diversity. Thus, we see that animals (repre- sented by Homo), plants (Zea), and fungi (Coprinus) (see blue arrows) constitute small and peripheral branches of even eukaryotic cellular diversity” (Cracraft and Donoghue, 2004). NOTE: The scale bar corresponds to 0.1 changes per nucleotide position. SOURCE: From Pace, N. R. 1997. A Molecular View of Microbial Diversity and the Biosphere. Science 276:734-740. Reprinted with permission from AAAS.

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WORKSHOP OVERVIEW 7 FIGURE WO-2  First glimpses of the microbial world. Panel A, Antonie van Leeuwenhoek was probably the first person to observe live microorganisms. Panel B, van Leeuwenhoek’s drawings of “animalcules” from the human mouth. SOURCE: Dobell (1932). Careful observation of microorganisms by scientists such as Louis Pasteur revealed the connections between microorganisms and practical phenomena. The production of beer and vinegar, for example, depended upon the presence of yeast for the conversion of sugar to alcohol and the fermentation of alcohol into acetic acid, respectively. Until the development of standardized culturing techniques in the late 19th century researchers could do little more than observe these creatures as a mixture of organisms in complex matrices. Pasteur also examined the con- nections between microorganisms and diseases of plants, animals, and humans, becoming an early proponent of the “germ theory” of disease (de Kruif, 1926). In 1884, Robert Koch and Friedrich Loeffler formalized the germ theory of disease by outlining a series of tests designed to determine whether a specific microorganism was the causative agent of a specific disease. These tests, known as Koch’s postulates (Box WO-1), required the isolation and propagation of “pure cultures” of microorganisms. Koch initially applied these tests to establish the infectious etiology of anthrax and tuberculosis (de Kruif, 1926). Using these techniques, researchers could conduct experimental investigations of specific microorganisms under controlled conditions. Our current understanding of microbe–host interactions have been influenced by more than a century of research, sparked by the germ theory of disease and rooted in historic notions of contagion that long preceded the research and intel- lectual syntheses of Pasteur and Koch in the 19th century (Lederberg, 2000). The success of this approach to the identification of the microbial basis of disease launched generations of “microbe hunters” who began a systematic search for disease-causing microbes that could be isolated and cultured under controlled laboratory conditions. Their work set a new course for the study and treatment of infectious disease-causing organisms. The “power and precision” of their studies

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8 THE SCIENCE AND APPLICATIONS OF MICROBIAL GENOMICS BOX WO-1 Koch’s Postulates 1.  The parasite occurs in every case of the disease in question and under cir- cumstances that can account for the pathological changes and clinical course of the disease. 2.  The parasite occurs in no other disease as a fortuitous and nonpathogenic parasite. 3.  After being fully isolated from the body and repeatedly grown in pure culture, the parasite can induce the disease anew. SOURCES: Fredericks and Relman (1996), Koch (1891), and Rivers (1937). using pure culture established these methods as the standard laboratory microbiol- ogy technique (Lederberg, 2000). At the same time, this disease-centric approach to microbe discovery has, for the past century and a half, not only influenced our collective perceptions of what microbes do “to” rather than “for” their hosts but also biased the database of the tree of life to one that, until relatively recently, has been focused almost entirely on disease-causing, culturable microorganisms. This pathogen-centric bias attributed disease entirely to the actions of in- vading microorganisms, thereby drawing battle lines between “them” and “us,” the injured hosts (Casadevall and Pirofski, 1999). Although it was recognized in Koch’s time that some microbes did not cause disease in previously exposed hosts (e.g., milk maids who had been exposed to cowpox did not become infected with smallpox), the fact that his postulates could not account for microbes that did not cause disease in all hosts was not generally appreciated until the arrival of vac- cines and the subsequent introduction of immunosuppressive therapies in the 20th century (Casadevall and Pirofski, 1999; Isenberg, 1988). By then, the paradigm of the systematized search for the microbial basis of disease, followed by the development of antimicrobial and other therapies to eradicate these pathogenic agents, had been firmly established in clinical practice. THE CULTIVATION BOTTLENECK, GENOMICS, AND THE UNIVERSAL TREE OF LIFE In the 1950s and 1960s this focus on a few easily cultured organisms pro- duced an explosion of information about microbial physiology and genetics that overshadowed efforts to understand the ecology and diversity of the microbial world (Pace, 1997). As the workhorses of the emerging field of molecular biol- ogy bacteria, such as Escherichia coli and Bacillus subtilis and their viruses (bacteriophages) became perhaps some of the best characterized microorganisms

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WORKSHOP OVERVIEW 9 FIGURE WO-3  The great plate count anomaly. SOURCE: Lewis (2011). Figure by Kim Lewis, Courtesy of Moselio Schaechter, Small things Considered, The Microbe Blog. in biological research. While a rich source of discovery and knowledge, this fo- cus on readily cultured organisms limited most researchers’ appreciation of the diversity and ubiquity of microbial life. The predisposition toward discovery, isolation, and characterization of mi- croorganisms that could be readily cultured4 in the laboratory is known as the “cultivation bottleneck” and is evident in the substantial difference in population counts of microorganisms present in a sample depending on whether they are con- ducted using microscopy or culturing techniques—a phenomenon known as the “great plate anomaly” (see Figure WO-3). This difference is attributed to the fact that the vast majority of microorganisms, 99 percent by some estimates, cannot be isolated and cultured5 using standard laboratory techniques (Handelsman, 2004). 4  The ease of isolation and culturing of certain organisms reflects an organism’s ability to grow rapidly into colonies on high-nutrient artificial growth media, typically under aerobic conditions. This had led some to characterize these species as the “weeds” of the microbial world (Hugenholtz, 2002). 5  Microorganisms may be unculturable because of the inability to replicate important nutritional or environmental requirements for growth, including the services provided by other microorganisms that may be present in natural settings.

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10 THE SCIENCE AND APPLICATIONS OF MICROBIAL GENOMICS SEQUENCE-BASED DETECTION AND DISCOVERY Pace and colleagues (1985) used sequence-based methods to investigate the composition of all constituents of the microbial biosphere. These culture-indepen- dent surveys led to the discovery of previously unknown and diverse lineages of organisms from habitats across the Earth, including bacterial and parasitic patho- gens in the human body (Handelsman, 2004; Pace, 1997; Relman et al., 1990; Santamaria-Fries et al., 1996). The polymerase chain reaction6 (PCR) technique, developed in 1983 by Kary Mullis, aided these studies by allowing researchers to easily amplify single copies of a particular DNA sequence into thousands or millions of copies. This advance enabled investigators to rapidly and comprehen- sively catalog the diversity of life forms in the microbial world. Initial molecular phylogeny studies demonstrated that this “unseen world” of microorganisms could be studied and confirmed that the number of organisms represented in the unculturable world far exceeded the size of the culturable world. While culture-based techniques remain the gold standard for disease de- tection, outbreak investigations, and infectious disease epidemiology, over the past several decades a range of sequence-based methods—including broad- range PCR, high-throughput sequencing technologies, microarrays, and shotgun metagenomics—have been applied to improve the detection and discovery of pathogens and other microorganisms. rRNA gene sequences may also be used to phylogenetically identify microbes that are otherwise uncharacterizable by other methods and approaches. Broad-Range PCR Some conserved genes and their encoded molecules have properties that render them useful as “molecular clocks.” These conserved genes, such as the 16S rRNA gene in bacteria, can be amplified from any member of a phylogenetic group using consensus primers.7 The sequences of the amplified, intervening gene regions with variable composition are then determined, in order to identify known or previously uncharacterized members of the group, and their evolutionary rela- tionships to all other organisms revealed. This approach has been used to discover previously uncharacterized bacterial, viral, and parasitic pathogens (Nichol et al., 1993; Relman, 1993, 1999, 2011; Relman et al., 1990, 1992). 6  The polymerase chain reaction (PCR) is a biochemical technology in molecular biology that amplifies a single or a few copies of a piece of DNA across several orders of magnitude, generating thousands to millions of copies of a particular DNA sequence. 7  Primers whose sequences are found in all known, and presumably unknown, members of the group.

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WORKSHOP OVERVIEW 11 High-Throughput Sequencing Technologies8 Nucleic acid sequencing technologies have dramatically enhanced our un- derstanding of the diversity of the microbiota and their dynamic interactions with the environments they reside in. The genomes of thousands of organisms from all three domains of life, as well as those of quasi-life forms such as viruses, have been sequenced. Metagenomics has taken this approach a step further by catalog- ing the genomic components of microbes living in complex environmental ma- trices, from soil samples, to the ocean, coral reefs, and the human body (Mardis, 2008). The conventional or first-generation technology of automated Sanger sequencing produced all of the early microbial sequence data. Next-generation 9 sequencing technologies, which were introduced in 2005, have decreased the cost and time necessary for sequence production. Sequence data have been used for a number of applications, including: • De novo assembly of entire genomes to produce primary genetic se- quences and to support the detailed genetic analysis of an organism. • Whole genome “resequencing” for the discovery of variants that differ in sequence to known genome sequences of a closely related strain. • Species classification and the identification of predicted coding sequences and novel gene discovery in genomic surveys of microbial communities (metagenomics). • “Seq-based” assays that determine the sequence content and abundance of mRNAs, non-coding RNAs, and small RNAs (collectively called RNA- seq); or measure genomewide profiles of DNA-protein complexes (ChIP- seq), methylation sites (methyl-seq), and DNase I hypersensitivity sites (DNase-seq) (Metzker, 2010). Microarrays Microarray technology runs the gamut from assays that contain hundreds to those containing millions of probes. Probes can be designed to distinguish differences in sequence variation that allow for pathogen speciation, or to detect thousands of agents across the tree of life. Arrays comprising longer probes (e.g., > 60 nucleotides) are more tolerant of sequence mismatches and may de- tect agents that have only modest similarity to those already known. Two longer probe array platforms are in common use for viral detection and discovery: the 8  Theseare large-scale methods to purify, identify, and characterize DNA, RNA, proteins, and other molecules. These methods are usually automated, allowing rapid analysis of very large numbers of samples. http://www.learner.org/courses/biology/glossary/through_put.html (accessed November 13, 2012). 9  As more advanced technologies are introduced, these technologies are sometimes referred to as “second generation” technologies. Nearly all current sequencing is “next generation” (i.e., not Sanger methodology).

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106 THE SCIENCE AND APPLICATIONS OF MICROBIAL GENOMICS FIGURE WO-47  Phylogenetic “dark matter” left to be sampled. SOURCE: Wu et al. (2009). Reprinted by permission from Macmillan Publishers Ltd: NATURE. Wu, D. et al. 2009. A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462:1056-1060, copyright 2009. For each subtree, taxa were sorted by their contribution to the subtree phylo- genetic diversity, and the cumulative phylogenetic diversity was plotted from maximal (left) to the least (right). The inset magnifies the first 1,500 organisms. Comparison of the plots shows the phylogenetic dark matter left to be sampled (Wu et al., 2009). Looking Forward “Once the diversity of the microbial world is catalogued, it will make astronomy look like a pitiful science.” —Julian Davies, Professor Emeritus, Microbiology and Immunology, University of British Columbia In order to maximize the discovery and characterization of new gene families and their associated novel functions, Wu et al., (2009) suggest that phylogenetic considerations should guide the selection of genomes for sequencing. By focusing on the novelty of an organism (highly divergent lineages of bacteria or archaea that lack representatives with sequenced genomes) the Genomic Encyclopedia of Bacteria and Archaea (GEBA) project seeks to “provide a phylogenetically bal- anced genomic representation of the microbial tree of life” (Wu et al., 2009). Se- quencing the genomes of 1,520 phylogenetically selected isolates could include half of the phylogenetic diversity represented by known cultured bacteria and

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WORKSHOP OVERVIEW 107 archaea. The sequencing of an additional 9,218 genome sequences from currently uncultured species could capture 50 percent of this subset of recognized diversity. According to Wu et al. (2009), “such an undertaking will require the development of new approaches to culturing or processing of multi-species samples using methods such as . . . physical isolation of cells from mixed populations followed by whole genome amplification methods.” The field of microbiology has made tremendous strides over the past several decades in describing the microbial world glimpsed for the first time just 300 years ago. Comparative genomic studies of bacterial species and metagenomic analyses of microbial communities to date have revealed how vastly we have underestimated the diversity, variability, and complexity of the microbial world. Microbial genomics offers the potential to efficiently characterize the vast cosmos of microbial diversity and rewrite the microbial community’s tree of life. Indeed, with the proliferation of culture-independent technologies and generation of enormous quantities of raw genomic sequences of microorganisms from diverse settings, the field of microbiology now suffers an “embarrassment of riches.” As observed in a recent editorial in Nature Reviews Microbiology (Editorial, 2011), “[t]he scale of life in the microbial world is such that amazing numbers become commonplace. These numbers can be sources of inspiration for those in the field and used to inspire awe in the next generation of microbiologists.” WORKSHOP OVERVIEW REFERENCES Achtman, M., G. Morelli, P. Zhu, T. Wirth, I. Diehl, B. Kusecek, A. J. Vogler, D. M. Wagner, C. J. Allender, W. R. Easterday, V. Chenal-Francisque, P. Worsham, N. R. Thomson, J. Parkhill, L. E. Lindler, E. Carniel, and P. Keim. 2004. Microevolution and history of the plague bacillus, Yersinia pestis. Proceedings of the National Academy of Sciences USA 101(51):17837-17842. Alagely, A., C. J. Krediet, K. B. Ritchie, and M. Teplitski. 2011. Signaling-mediated cross-talk modu- lates swarming and biofilm formation in a coral pathogen Serratia marcescens. International Society for Microbial Ecology Journal 5(10):1609-1620. Alm, E. 2012. Session I: The Application of Computational/Theoretical and Experimental Approaches to Study the Evolution of Microorganisms. Paper presented at the Forum on Microbial Threats Workshop, The Science and Applications of Microbial Genomics, Washington, DC, Institute of Medicine, Forum on Microbial Threats, June 12. Baz, M., Y. Abed, J. Papenburg, X. Bouhy, M. E. Hamelin, and G. Boivin. 2009. Emergence of oseltamivir-resistant pandemic H1N1 virus during prophylaxis. New England Journal of Medi- cine 361(23):2296-2297. Bentley, S. 2009. Sequencing the species pan-genome. Nature Reviews Microbiology 7:258-259. Berglund, E. C., B. Nystedt, S. G. E. Andersson. 2009. Computational resources in infectious disease: Limitations and challenges. PLoS Computational Biology 5(10):e1000481. Blaser, M. 1997. Ecology of Helicobacter pylori in the human stomach. Journal of Clinical Investiga- tion 100(4):759-762. Budowle, B. 2012. Session IV: Microbial Forensics. Paper presented at the Forum on Microbial Threats Workshop, The Science and Applications of Microbial Genomics, Washington, DC, Institute of Medicine Forum on Microbial Threats, June 13. Bos, K. I., V. J. Schuenemann, G. B. Golding, H. A. Burbano, N. Waglechner, B. K. Coombes, J. B. McPhee, S. N. DeWitte, M. Meyer, S. Schmedes, J. Wood, D. J. Earn, D. A. Herring, P. Bauer, H. N. Poinar, and J. Krause. 2011. A draft genome of Yersinia pestis from victims of the Black Death. Nature 478(7370):506-510.

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