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Workshop Overview1

Perhaps one of the most important changes we can make is to supersede the 20th-century metaphor of war for describing the relationship between people and infectious agents. A more ecologically informed metaphor, which includes the germs’-eye view of infection, might be more fruitful. Consider that microbes occupy all of our body surfaces. Besides the disease-engendering colonizers of our skin, gut, and mucous membranes, we are host to a poorly cataloged ensemble of symbionts to which we pay scant attention. Yet they are equally part of the superorganism genome with which we engage the rest of the biosphere.

—Joshua Lederberg, “Infectious History” (2000)

MICROBIAL ECOLOGY IN STATES OF HEALTH AND DISEASE

Introduction

Individually and collectively, resident microbes play important roles in host health and survival. Shaping and shaped by their host environments, these microorganisms form intricate communities that are in a state of dynamic equilibrium.

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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 Charlee Alexander, 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 Forum, the Institute of Medicine, or the National Research Council, and they should not be construed as reflecting any group consensus.



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Workshop Overview1 Perhaps one of the most important changes we can make is to supersede the 20th-century metaphor of war for describing the relationship between people and infectious agents. A more ecologically informed metaphor, which includes the germs’-eye view of infection, might be more fruitful. Consider that microbes occupy all of our body surfaces. Besides the disease-engendering colonizers of our skin, gut, and mucous membranes, we are host to a poorly cataloged ensemble of symbionts to which we pay scant attention. Yet they are equally part of the superorganism genome with which we engage the rest of the biosphere. —Joshua Lederberg, “Infectious History” (2000) MICROBIAL ECOLOGY IN STATES OF HEALTH AND DISEASE Introduction Individually and collectively, resident microbes play important roles in host health and survival. Shaping and shaped by their host environments, these micro- organisms form intricate communities that are in a state of dynamic equilibrium. 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 Charlee Alexander, 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 Forum, the Institute of Medicine, or the National Research Council, and they should not be construed as reflecting any group consensus. 1

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2 MICROBIAL ECOLOGY IN STATES OF HEALTH AND DISEASE This ecologic and dynamic view of host–microbe interactions is rapidly redefin­ ing our view of health and disease. It is now accepted that the vast majority of microbes are, for the most part, not intrinsically harmful, but rather become established as persistent, co-adapted colonists in equilibrium with their environ- ment, providing useful goods and services to their hosts while deriving benefits from these host associations. Disruption of such alliances may have consequences for host health, and investigations in a wide variety of organisms have begun to illuminate the complex and dynamic network of interactions—across the spec- trum of hosts, microbes, and environmental niches—that influence the formation, function, and stability of host-associated microbial communities (Dethlefsen et al., 2007; Turnbaugh et al., 2007; Robinson et al., 2010; IOM, 2012). From the microbiota2 on the surface of our skin to those that inhabit the mucus-covered lining of our gut, we are deeply embedded in a microbial world— an observation that extends to most, if not all, plant and animal life on Earth. By the time we reach adulthood, more than 100 trillion microorganisms—including Archaea, Bacteria, Fungi, Protozoa, and Viruses—inhabit specialized environ- mental niches in and on our body surfaces, forming complex communities that contribute to the nutrition, defense, and development of the intricate, microbe- dominated eco­ystems that we humans call “ourselves.” Indeed, we are more s accurately viewed as superorganisms—compilations composed of human and mi- crobial cells that are “yoked into a chimera of sorts’” (Lederberg, 2000; Hooper and Gordon, 2001; Xu and Gordon, 2003). Recent studies of the human gut microbiota have suggested intriguing asso­ ciations between “dysbiosis” (a general term3 denoting alterations to the com- position and dynamics of our microbiota) and a variety of chronic conditions not thought to have a microbial etiology—including severe acute malnutrition, obesity, cardiovascular disease, asthma, adult-onset diabetes, and the inflam- matory bowel diseases (Ley et al., 2005; Petersen et al., 2008; Han et al. 2012; Karlsson et al., 2012, 2013; Qin et al., 2012; Ridaura et al., 2013; Smith et al., 2013; Tang et al., 2013). Scientists have yet to determine whether these associa- tions reflect a causal relationship, and many have urged caution about “oversell- ing” the importance of these initial observations. Still, the dramatic rise in the global pervasiveness of many of these apparently noncommunicable diseases over the past half-century has fueled intense interest in the possibility that lo- cal and global alterations in our microbial ecology may be contributing to the 2   For the purposes of this workshop overview, microbiota is a collection of microorganisms—­ including Archaea, Bacteria, Fungi, Protozoa, and Viruses—that exist in the same place at the same time (see Robinson et al., 2010). The terms resident, endogenous, or indigenous microorganisms describe host-associated microbiota. 3   Coined by Mechnikoff in the early 1900s, dysbiosis describes a state of microbial imbalance in the gut and now refers to a change in the structural and/or functional configuration of the microbiota that produces a disruption in the homeostasis between a host and its indigenous microbes (Gordon, 2012).

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WORKSHOP OVERVIEW 3 development or progression of a wide variety of complex diseases (Blaser and Falkow, 2009). In addition to the varied landscapes provided by animals and plants, micro- bial communities inhabit Earth’s soil, water, and air, where they drive important geochemical and biological processes. Indeed, microbial communities form the “heart of all ecosystems” (Shade et al., 2012), and their exploration promises to transform our understanding of the natural world (IOM, 2006, 2009, 2012; Shade et al., 2012). Taking a more holistic view of “who [and what] we are” that includes consideration of the role that our resident microbiota plays in influenc- ing states of health and disease may also revolutionize clinical approaches to the diagnosis, treatment, and, ultimately, prevention of disease (Shade et al., 2012). Statement of Task On March 18 and 19, 2013, the Institute of Medicine’s (IOM’s) Forum on Microbial Threats hosted a public workshop, in Washington, DC, to explore the scientific and therapeutic implications of microbial ecology in states of health and disease. Participants explored host–microbe interactions in humans, animals, and plants; emerging insights into how microbes may influence the development and maintenance of states of health and disease; the effects of environmental change(s) on the formation, function, and stability of microbial communities; and research challenges and opportunities for this emerging field of inquiry. This meeting built and expanded upon many of the topics explored at a 2002 Forum workshop, The Infectious Etiology of Chronic Diseases (IOM, 2004). 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 commen- tary. The contents of the unattributed sections of this summary report provide a technical context for the reader to appreciate the presentations and discussions that occurred over the 2 days of this workshop and do not represent the views of the members of the Forum on Microbial Threats, its sponsors, or the IOM. The summary is organized into sections as a topic-by-topic distillation 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 workshop participants may be found, in alphabeti- cal order by author, in Appendix A. Although this workshop summary provides a description 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

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4 MICROBIAL ECOLOGY IN STATES OF HEALTH AND DISEASE and perspectives that 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. HUMANS, ANIMALS, AND PLANTS IN A MICROBIAL WORLD Co-evolution, co-adaptation, and codependency are all features of our relationships with our indigenous microbiota. —Blaser and Falkow (2009) Like all forms of life on Earth, microorganisms exist within often complex communities. In every habitat studied—from acidic hot springs to the external and internal surfaces of plants, animals, and humans—microorganisms interact with and influence one another and their environment (IOM, 2012). As noted by David Relman, chair of the Forum on Microbial Threats, the important biology accomplished by the net actions of interacting microbial communities is really the norm on our planet, yet we are only just beginning to explore and ­ ppreciate a the principles that might define these communities. Most studies of the microbial world, until fairly recently, isolated micro­ organisms from their natural ecological settings and studied in sterile mono- culture.4 Guided by a reductionist strategy of reductionism that relied upon the isolation and growth of single microbial species in pure culture, this approach limited observations to a narrow range of species that could be isolated and grown under controlled conditions5 (IOM, 2012). Molecular, sequence-based approaches6—pioneered by environmental microbiologists in the late 20th cen- tury—ultimately alleviated these constraints and allowed scientists to characterize communities of bacteria and Archaea in a wide range of environments. These studies dramatically expanded our understanding of the natural world by reveal- ing the vast, and previously unseen, diversity of the microbial world (Pace, 1997; Whitman et al., 1998; Handelsman, 2004). Today, genomic methods are being 4   Most studies of microbes were performed on organisms isolated in the laboratory and apart from their natural environmental contexts. 5   Culturing single cells of a particular microbial type is a useful approach to learn about the biol- ogy of a particular organism. It is an unnatural environment for most microorganisms because cells are grown in isolation and under controlled conditions. However, by some estimates greater than 99 percent of the microbial world is or may be unculturable (Robinson et al., 2010). 6   Because all cell-based organisms possess rRNA genes, these gene sequences were used as a culture-independent means for organism detection. Researchers used sequences shared by all rRNA it is an unnatural environment for most microorganisms because to amplify each rRNA gene sequence present in a sample and then analyzed subtle differences between rRNA gene sequences to infer the types of organisms present. Today, sequence-based techniques can be applied directly to DNA isolated from an environmental sample to characterize entire genomes of organisms present (Eisen, 2007).

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WORKSHOP OVERVIEW 5 developed to extend these ecological surveys to fungi and viruses (see Virgin et al., 2009; Findley et al., 2013). Over the past decade, investigations of the ecology of host-associated mi- crobial communities in a variety of contexts have flourished because of the lower cost, increased speed, and greater capacities of nucleic acid sequencing and other analytic techniques, coupled with advances in bioinformatics and computational biology. In addition to metagenomic surveys of the taxa and genomic content present in a microbial community (discovering “who is there?”), it is increasingly possible to examine their function (“what are they doing and why are they doing it?”) by probing gene expression (metatranscriptomics), protein synthesis (pro- teomics), and production of small molecular weight compounds (metabolomics). Coupling these techniques with concepts developed in the field of macroecology, r ­esearchers are able to create a rich, multidimensional picture of the ecology of microbial communities (Robinson et al., 2010; Boyle and Gill, 2012). Terminol- ogy commonly used in these studies are defined in Table WO-1. Microbes in a Microbial World: Exploring Host–Microbe Ecosystems The idea that disruption of host–microbe interactions or alterations to com- munity structure may lead to disease raises fundamental questions about the ways in which host–microbe, and microbe–microbe, associations are formed and maintained. Such questions have been the basis of a rich body of research on sym- biotic interactions, in which disparate organisms form beneficial (mutualistic), neutral (commensal), or harmful (parasitic) associations that often persist over the lifetime of the host. While such symbiotic associations were once considered to be exceptions, symbioses are now known to be the rule in biotic and abiotic systems. Microbial symbionts are not only a normal part of the life cycle of plants and animals, they are often integral to host development and evolution (Fraune and Bosch, 2010; Gilbert et al., 2012). Studies of symbioses in a wide variety of organisms have provided im- portant insights into the factors that drive the formation, function, and stability of host–­ icrobe associations and a means to pursue the deeper question of m whether universal rules and mechanisms govern these processes (IOM, 2009, 2012; Fraune and Bosch, 2010). As noted by Forum member Margaret McFall- Ngai of University of Wisconsin, Madison, “Nature and evolution have done phenomenal experiments from which we can learn, and although humans often forget that they are part of the environment, we are . . . highly linked, and, more importantly, we are products of our evolutionary history.” McFall-Ngai went on to observe that comparative investigations of host–microbe associations in a variety of systems will help to define the “very basic rules by which animals and plants interact with microorganisms.”

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6 MICROBIAL ECOLOGY IN STATES OF HEALTH AND DISEASE TABLE WO-1  Microbial Ecology Definitions Term Definition Biogeography The study of biodiversity in space and time Diversity A measure of how much variety is present in a community, irrespective of the identities of the organisms present; consists of richness and evenness Evenness The distribution of individuals across types Function An activity or “behavior” associated with a community (e.g., nitrogen fixation or resistance to invasion) Invasion An ecological event characterized by the establishment of a foreign organism in a new community and the persistence and spread of this organism Metagenomics A culture-independent method used for functional and sequence- based analysis of total environmental (community) DNA (note that this is not the same as amplifying, cloning, and sequencing the 16S rRNA-encoding gene, although metagenomic sequences, such as those generated via modern sequencing methods, can be probed for 16S rRNA-encoding genes or other phylogenetic markers) Microbiome The gene complement of a community Microbiota/community A collection of microorganisms existing in the same place at the same time Resilience The rate at which a community recovers to its native structure following a perturbation Resistance The ability of a community to resist change to its structure after an ecological challenge Richness Number of types (e.g., species) in a community Similarity A measure that determines the similarity of two or more communities, typically based on shared members, total richness, and sometimes abundance of members Structure The composition of the community and the abundance of individual members Temporal stability The ability of a community to maintain its native structure SOURCE: Robinson et al. (2010). Examples of Host–Microbe Communication, Colonization, and Development Symbiotic associations can be quite specific, as illustrated in the following examples, suggesting co-evolution of host and microbe over long periods of time. This shared evolutionary past is also reflected in the chemical dialog that mediates these associations (McFall-Ngai et al., 2013). In addition to long-term selective forces that hone microbe–host interdependencies, indigenous microbes are subject to shifting environmental conditions over the lifetime of the host. Early patterns of niche colonization and community assembly can strongly— and in some cases, irreversibly—influence the developing host environment and microbiota.

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WORKSHOP OVERVIEW 7 The bacterium and the squid  Studied for more than 25 years, the persistent association between the Hawaiian bobtail squid Euprymna scolopes and the gram-negative, luminescent bacterium Vibrio fischeri continues to reveal impor- tant insights into host–microbe associations. An early and exclusive association between the squid and a single species of bacteria (V. fischeri) triggers tissue maturation within the squid’s body cavity to form a specialized light-emitting organ. Luminescence emitted by the bacteria resembles moonlight and starlight filtering through ocean waters, camouflaging the squid from predators swimming below (Nyholm and McFall-Ngai, 2004). Bacterial colonization begins within hours of the squid’s hatching (Fig- ure WO-1). The squid acquires V. fischeri from its environment, and upon the initiation of colonization the juvenile squid selectively recruits V. fischeri in a glycan-rich mucus, separating it from the rich mixture of seawater microbes. It has now been reported that first contact within the squid-vibrio symbiosis triggers profound molecular and chemical changes that are crucial for bacterial colonization7 (­ remer et al., 2013). Once colonized, the squid undergoes dra- K matic morphological changes—including programmed cell death that eliminates “symbiont-recruiting” structures and the remodeling of tissue to favor the mainte- nance of V. fischeri within the mature light organ. Host tissue recognition of two non-specific bacterial products—peptidoglycan and lipopolysaccharide—triggers theses developmental events in the squid (Nyholm and McFall-Ngai, 2004). These molecules are members of a broad class of microbe-associated ­ olecular m patterns8 (MAMPs) that have now been shown to trigger developmental pro- cesses in a wide variety of animals and plants (see Koropatnick et al., 2004, and M ­ cFall-Ngai et al., 2013). Plant–microbe interactions in the rhizosphere  Like the development of the bobtail squid’s light organ, one of the best-characterized plant–microbe inter­ actions features a symbiotic association that triggers tissue development in leguminous plants. Nitrogen-fixing bacteria called rhizobia, attracted by plant- secreted flavonoid compounds, colonize legume roots and release chemicals called nodulation (Nod) factors. These factors trigger gene expression within plant roots that results in the uptake of bacteria by plant tissues to form root n ­ odules. The captured bacteria provide a critical nutrient for the plant and in 7   This exquisitely sensitive response to the host’s specific symbiotic partner includes the upregula- tion of a host endochitinase, whose activity hydrolyzes polymeric chitin in the mucus into chitobiose, thereby priming the symbiont and also producing a hemoattractant gradient that promotes V. fischeri migration into host tissues. Thus, the host responds transcriptionally upon initial symbiont contact, which facilitates subsequent colonization (Kremer et al., 2013). 8   Microbe-associated molecular patterns (MAMPs) are essential structures on features of microbes that are recognized by the innate immune system (Koropatnick et al., 2004). They are recognized by toll-like receptors (TLRs) and other pattern-recognition receptors (PRRs) in plants and animals. MAMPs are often referred to as pathogen-associated molecular patterns (PAMPs). However these motifs are shared among microbes.

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8 MICROBIAL ECOLOGY IN STATES OF HEALTH AND DISEASE FIGURE WO-1  Model for early colonization. (A) The initial contact of V. fischeri with host tissues induces the expression of several genes (e.g., proteases, chitinases such as EsChitotriosidase, and lysozyme) whose products, when supplemented with components already present in the mucus (NO and EsPGRP2), affect the chemistry of the mucus matrix, shaping the specificity and preparing for future colonization events. (B) Course of events that allow selective colonization by V. fischeri. Left: Antimicrobial compounds (e.g., lysozyme and PGRP2) are activated by acidic proteases in the low-pH environment and participate in the selective exclusion of nonsymbiotic bacteria. Right: While V. fischeri cells are “pausing” in the aggregate, the upregulation of EsChitotriosidase in the ciliated field of the light organ hydrolyzes chitin into chitobiose, which prepares V. fischeri to sense and be attracted toward chitobiose. (C) EsChitotriosidase, which is highly expressed close to the pores and optimally active at low pH, degrades chitin produced by the host into chitobiose, thereby establishing a chitobiose gradient extending out of the pores. Primed V. fischeri cells are attracted by the chitobiose gradient and migrate through the pores (Mandel et al., 2012). SOURCE: Mandel et al. (2012) in Kremer et al. (2013).

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WORKSHOP OVERVIEW 9 return are fed by the plant’s roots. The roots of most higher-plant species form similar, flavonoid-mediated symbiotic associations with mycorrhizal fungi (IOM, 2006, 2009; Desbrosses and Stougaard, 2011). Distinct microbiota colonize the rhizosphere (root–soil interface) and endo- sphere (endophytic compartment within plant root tissues), both of which differ in composition from those found in the surrounding soil. Plant roots provide a struc- tured and nonhomogeneous habitat for tens of thousands of species of ­ icrobes. m Within this complex environment, microhabitats of nutrient, water, pH, and oxygen gradients shape—and are shaped by—root-associated microbial commu- nities (Ramirez-Puebla et al., 2013). Explorations of this complex environment have illuminated a variety of small molecules (including MAMPs) and chemical signaling networks that mediate plant–microbe and microbe–microbe interac- tions. The intricate chemical and genetic “cross-talk” between plants and their associated microbiota supports a variety of functions—including plant growth, nutrition, productivity, carbon sequestration, phytoremediation,9 and protection (Figure WO-2) (Badri et al., 2009; Berendsen et al., 2012; Bulgarelli et al., 2012). Community Assembly and Dynamics in a Model Vertebrate Microbial colonization is a crucial event in the development of the vertebrate gut, and early colonization events appears to be important to the normal matu- ration and functioning of the immune and digestive systems. In a recent study in the Proceedings of the National Academy of Sciences of the United States of America, Everard et al. (2013) appear to have demonstrated a causal relationship between ­ kkarmansia carriage and obesity. Speakers Karen Guillemin and Bren- A dan ­ ohannan, both of the University of Oregon, described wide-ranging work B with the zebrafish Danio rerio, which Guillemin described as “a model vertebrate that is allowing us to explore the complex systems biology of host–microbe in- teracting systems” (Dr. Guillemin’s contribution may be found on pages 323-346 in Appendix A; Dr. Bohannan’s contribution may be found on pages 164-184 in Appendix A). Zebrafish have several advantages as a model system, Guillemin explained: their guts and immune systems resemble those of other mammals, including humans; they develop rapidly; they are transparent, so their digestive tract can be easily visualized; they are readily amenable to genetic manipulation; and, perhaps most importantly, germ-free zebrafish have been developed, along with methods to associate them with different bacterial communities. Patterns of colonization  Guillemin described her use of germ-free zebra­ sh and fi methods to associate them with different bacterial communities. “What our models allow us to do is to build up these systems and look at increasing complexity, start- ing with the germ-free animal,” she said. “We can then associate them with very 9   The use of green plants to decontaminate polluted soil or water.

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10 MICROBIAL ECOLOGY IN STATES OF HEALTH AND DISEASE FIGURE WO-2  Illustration of the chemical communication that exists between plant roots and other organisms in the complex rhizosphere. Plant roots secrete a wide range of compounds; among those are sugars and amino acids that are engaged in attracting (chemo­axis) microbes (1), flavonoids act as signaling molecules to initiate interactions t with mycorrhiza (AM fungi) (2), rhizobium and (3) pathogenic fungi (oomycetes) (4), a ­ liphatic acids (e.g., malic acid) are involved in recruiting specific plant growth promoting rhizobacteria (Bacillus subtilis) (5), nematodes secrete growth regulators (cytokinins) that are involved in establishing feeding sites in plant roots (6), and nematodes secrete other compounds (organic acids, amino acids, and sugars) involved in attracting bacteria and in bacterial quorum sensing (7). Knowledge of the roles of other types of compounds, such as fatty acids (8) and proteins (9), secreted by roots in the rhizosphere and other multipartite interactions (10), remains unknown. SOURCE: Badri et al. (2009). simple communities, or we can allow them to be colonized with complex natural communities . . . [to] look at this whole spectrum of complexity” (Figure WO-3). The recently developed light sheet microscope provides ­ uillemin and coworkers G with high-resolution, real-time imaging of the colonization and growth of bacteria in the developing zebrafish gut (Taormina et al., 2012).

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WORKSHOP OVERVIEW 11 FIGURE WO-3 Host–microbe systems biology. In germ-free model systems, micro- bial associations may be manipulated to explore host–microbe interactions of increasing complexity. Gnotobiology comprises the study of germ-free plants and animals, as well as living things in which specific microorganisms, added by experimental methods, are known to be present. SOURCE: Guillemin (2013). Using this method in germ-free animals, the researchers observed that “early colonizers”—those bacteria that first reach the digestive tract—tend to dominate the developing community (Guillemin and Parthasarathy, unpublished). “We’re exploring the possibility that those first colonizers might have access to certain privileged niches within the gut, and . . . whether there are changes in bacterial physiology upon colonization, perhaps in conjunction with changes in the host environment upon colonization,” she said. Dynamic interactions  Bacterial colonization of the zebrafish gut triggers an innate immune response by the host, in the form of neutrophils—which are not present in the intestinal tracts of germ-free fish, Guillemin noted (Bates et al., 2007). Through experiments in which different species of bacteria that naturally populate the zebrafish gut were individually introduced to germ-free animals, she and coworkers found that the host response (as measured by neutrophil influx) was both varied and species specific; some isolates were very pro-inflammatory, inducing a large number of neutrophils, while others had very little effect on the

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