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Microbial Ecology in States of Health and Disease
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. This ecologic and dynamic view of host-microbe interactions is rapidly redefining 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 environment, 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 interaction - across the spectrum of hosts, microbes, and environmental niches - that influence the formation, function, and stability of host-associated microbial communities.
Microbial Ecology in States of Health and Disease is the summary of a workshop convened by the Institute of Medicine's Forum on Microbial Threats in March 2013 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.
eBook
Plant–microbiome interactions: from community assembly to plant health
Healthy plants host diverse but taxonomically structured communities of microorganisms, the plant microbiota, that colonize every accessible plant tissue. Plant-associated microbiomes confer fitness advantages to the plant host, including growth promotion, nutrient uptake, stress tolerance and resistance to pathogens. In this Review, we explore how plant microbiome research has unravelled the complex network of genetic, biochemical, physical and metabolic interactions among the plant, the associated microbial communities and the environment. We also discuss how those interactions shape the assembly of plant-associated microbiomes and modulate their beneficial traits, such as nutrient acquisition and plant health, in addition to highlighting knowledge gaps and future directions.In this Review, Trivedi and colleagues explore the interactions between plants, their associated microbial communities and the environment, and also discuss how those interactions shape the assembly of plant-associated microbiomes and modulate their beneficial traits.
Journal Article
Salmonella manipulates the host to drive pathogenicity via induction of interleukin 1beta
Acute gastrointestinal infection with intracellular pathogens like Salmonella Typhimurium triggers the release of the proinflammatory cytokine interleukin 1[beta] (IL-1[beta]). However, the role of IL-1[beta] in intestinal defense against Salmonella remains unclear. Here, we show that IL-1[beta] production is detrimental during Salmonella infection. Mice lacking IL-1[beta] (IL-1[beta] .sup.-/-) failed to recruit neutrophils to the gut during infection, which reduced tissue damage and prevented depletion of short-chain fatty acid (SCFA)-producing commensals. Changes in epithelial cell metabolism that typically support pathogen expansion, such as switching energy production from fatty acid oxidation to fermentation, were absent in infected IL-1[beta] .sup.-/- mice which inhibited Salmonella expansion. Additionally, we found that IL-1[beta] induces expression of complement anaphylatoxins and suppresses the complement-inactivator carboxypeptidase N (CPN1). Disrupting this process via IL-1[beta] loss prevented mortality in Salmonella-infected IL-1[beta] .sup.-/- mice. Finally, we found that IL-1[beta] expression correlates with expression of the complement receptor in patients suffering from sepsis, but not uninfected patients and healthy individuals. Thus, Salmonella exploits IL-1[beta] signaling to outcompete commensal microbes and establish gut colonization. Moreover, our findings identify the intersection of IL-1[beta] signaling and the complement system as key host factors involved in controlling mortality during invasive Salmonellosis.
Journal Article
The gut microbiota–brain axis in behaviour and brain disorders
In a striking display of trans-kingdom symbiosis, gut bacteria cooperate with their animal hosts to regulate the development and function of the immune, metabolic and nervous systems through dynamic bidirectional communication along the ‘gut–brain axis’. These processes may affect human health, as certain animal behaviours appear to correlate with the composition of gut bacteria, and disruptions in microbial communities have been implicated in several neurological disorders. Most insights about host–microbiota interactions come from animal models, which represent crucial tools for studying the various pathways linking the gut and the brain. However, there are complexities and manifest limitations inherent in translating complex human disease to reductionist animal models. In this Review, we discuss emerging and exciting evidence of intricate and crucial connections between the gut microbiota and the brain involving multiple biological systems, and possible contributions by the gut microbiota to neurological disorders. Continued advances from this frontier of biomedicine may lead to tangible impacts on human health.In this Review, Morais, Schreiber and Mazmanian discuss emerging and exciting evidence of intricate and potentially important connections between the gut microbiota and the brain involving multiple biological systems, and possible contributions by the gut microbiota to complex behaviours.
Journal Article
Large-scale association analyses identify host factors influencing human gut microbiome composition
To study the effect of host genetics on gut microbiome composition, the MiBioGen consortium curated and analyzed genome-wide genotypes and 16S fecal microbiome data from 18,340 individuals (24 cohorts). Microbial composition showed high variability across cohorts: only 9 of 410 genera were detected in more than 95% of samples. A genome-wide association study of host genetic variation regarding microbial taxa identified 31 loci affecting the microbiome at a genome-wide significant (
P
< 5 × 10
−8
) threshold. One locus, the lactase (
LCT
) gene locus, reached study-wide significance (genome-wide association study signal:
P
= 1.28 × 10
−20
), and it showed an age-dependent association with
Bifidobacterium
abundance. Other associations were suggestive (1.95 × 10
−10
<
P
< 5 × 10
−8
) but enriched for taxa showing high heritability and for genes expressed in the intestine and brain. A phenome-wide association study and Mendelian randomization identified enrichment of microbiome trait loci in the metabolic, nutrition and environment domains and suggested the microbiome might have causal effects in ulcerative colitis and rheumatoid arthritis.
Analysis of human genotypes and 16S microbiome data of 18,473 individuals from 25 cohorts through a genome-wide association study, a phenome-wide association study and Mendelian randomization identifies host genetic and microbial trait associations.
Journal Article
You are what you eat: diet, health and the gut microbiota
Since the renaissance of microbiome research in the past decade, much insight has accumulated in comprehending forces shaping the architecture and functionality of resident microorganisms in the human gut. Of the multiple host-endogenous and host-exogenous factors involved, diet emerges as a pivotal determinant of gut microbiota community structure and function. By introducing dietary signals into the nexus between the host and its microbiota, nutrition sustains homeostasis or contributes to disease susceptibility. Herein, we summarize major concepts related to the effect of dietary constituents on the gut microbiota, highlighting chief principles in the diet–microbiota crosstalk. We then discuss the health benefits and detrimental consequences that the interactions between dietary and microbial factors elicit in the host. Finally, we present the promises and challenges that arise when seeking to incorporate microbiome data in dietary planning and portray the anticipated revolution that the field of nutrition is facing upon adopting these novel concepts.
Journal Article
Prevotella diversity, niches and interactions with the human host
The genus Prevotella includes more than 50 characterized species that occur in varied natural habitats, although most Prevotella spp. are associated with humans. In the human microbiome, Prevotella spp. are highly abundant in various body sites, where they are key players in the balance between health and disease. Host factors related to diet, lifestyle and geography are fundamental in affecting the diversity and prevalence of Prevotella species and strains in the human microbiome. These factors, along with the ecological relationship of Prevotella with other members of the microbiome, likely determine the extent of the contribution of Prevotella to human metabolism and health. Here we review the diversity, prevalence and potential connection of Prevotella spp. in the human host, highlighting how genomic methods and analysis have improved and should further help in framing their ecological role. We also provide suggestions for future research to improve understanding of the possible functions of Prevotella spp. and the effects of the Western lifestyle and diet on the host–Prevotella symbiotic relationship in the context of maintaining human health.Prevotella is a genus of bacteria that commonly associate with humans, in various body sites. In this Review, Segata, Ercolini and colleagues discuss Prevotella diversity and the evidence for the involvement of these bacteria in human health and disease.
Journal Article
The role of plant growth promoting rhizobacteria in plant drought stress responses
Climate change has exacerbated the effects of abiotic stresses on plant growth and productivity. Drought is one of the most important abiotic stress factors that interfere with plant growth and development. Plant selection and breeding as well as genetic engineering methods used to improve crop drought tolerance are expensive and time consuming. Plants use a myriad of adaptative mechanisms to cope with the adverse effects of drought stress including the association with beneficial microorganisms such as plant growth promoting rhizobacteria (PGPR). Inoculation of plant roots with different PGPR species has been shown to promote drought tolerance through a variety of interconnected physiological, biochemical, molecular, nutritional, metabolic, and cellular processes, which include enhanced plant growth, root elongation, phytohormone production or inhibition, and production of volatile organic compounds. Therefore, plant colonization by PGPR is an eco-friendly agricultural method to improve plant growth and productivity. Notably, the processes regulated and enhanced by PGPR can promote plant growth as well as enhance drought tolerance. This review addresses the current knowledge on how drought stress affects plant growth and development and describes how PGPR can trigger plant drought stress responses at the physiological, morphological, and molecular levels.
Highlight
This review aims to highlight the recent advances in understanding the effects of plant growth-promoting rhizobacteria in enhancing plant growth and drought stress tolerance.
Journal Article
Current understanding of the human microbiome
Our understanding of the link between the human microbiome and disease, including obesity, inflammatory bowel disease, arthritis and autism, is rapidly expanding. Improvements in the throughput and accuracy of DNA sequencing of the genomes of microbial communities that are associated with human samples, complemented by analysis of transcriptomes, proteomes, metabolomes and immunomes and by mechanistic experiments in model systems, have vastly improved our ability to understand the structure and function of the microbiome in both diseased and healthy states. However, many challenges remain. In this review, we focus on studies in humans to describe these challenges and propose strategies that leverage existing knowledge to move rapidly from correlation to causation and ultimately to translation into therapies.
Journal Article