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One of the most revolutionary advances in the biological sciences in recent years has been the realization that microbial communities occupy virtually every environment and have central roles in human health and disease, as well as in the biogeochemical processes that sustain life on our planet. Moving beyond cataloguing the species and genes that are present in these diverse environments, the microbiome field is now focusing on defining the mechanisms underpinning the interactions between microorganisms and their environment. One of the main goals is to elucidate how the composition and functions of the human microbiota influence the initiation and progression of important human diseases, such as diabetes and cancer, with a view towards improving their diagnosis and treatment. Progress in the field has been driven by multi'omic technologies, combined with new computational tools and models to interpret the vast complexity of this fascinating research area.
In this series of articles, Nature Reviews Microbiology explores the latest developments in the study of environmental and host-associated microbiomes, highlighting the tools and methods that are propelling the field forward, the novel mechanistic insights into the composition and functions of these microbial communities, and the complex interplay between the microbiota and its surroundings.
The human body hosts vast numbers of different viruses, collectively termed the virome. In this Review, Liang and Bushman provide an overview of research on the human virome and highlight recent studies that explore the assembly and composition of the human virome as well as host–virome interactions in health and disease.
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.
Viruses are extremely diverse and not all of this diversity has been captured so far. In this Review, Martínez Martínez, Martinez-Hernandez and Martinez-Garcia explore the potential and limitations of single-virus genomics and how this emerging technology can complement other methods.
In this Review, Fan and Pedersen discuss how the gut microbiota and derived microbial compounds may contribute to human metabolic health and to the pathogenesis of common metabolic diseases, and highlight examples of microbiota-targeted interventions aiming to optimize metabolic health.
The gut microbiota contributes to host physiology through the production of a myriad of metabolites. In this Review, Bäckhed and colleagues discuss the major classes of microbial metabolites, highlight examples of how microbial metabolites affect host health and provide a potential framework for integration of discovery-based metabolite studies with mechanistic work.
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.
The archaeal community, the archaeome, is now increasingly recognized as an important component of host-associated microbiomes. In this Review, Moissl-Eichinger and colleagues discuss the diversity and potential roles of the archaea associated with protists, plants and animals, highlighting the potential roles of archaea in human health and disease.
Large-scale metagenomic analyses are vastly increasing the rate of discovery of variation within species but they are also leading to scientific and semantic challenges. Bork and colleagues highlight the advances and challenges that are resulting from the use of metagenomic data to study within-species diversity.
In this Review, Ruff, Greiling and Kriegel discuss the mechanisms through which the microbiota contributes to the predisposition, initiation and perpetuation of immune-mediated diseases, and explore the therapeutic avenues that either target the microbiota, the barrier surfaces or the host immune system to restore tolerance and homeostasis.
The schooner Tara sailed 140,000 km across the global oceans to sample diverse marine ecosystems and plankton communities. In the Review, members of the Tara Oceans project highlight how resulting data can be used for an integrated understanding of ocean biology.
In this Review, Hatzenpichler et al. introduce next-generation physiology, which is a suite of new techniques that enable investigation into the phenotypes of individual cells in a non-destructive manner. Next-generation physiology complements genomics and culturing and provides new insights into microbiome function.
In this Review, Jansson and Hofmockel explore the impacts of climate change on soil microorganisms in different climate-sensitive soil ecosystems and the potential ways that soil microorganisms can be harnessed to help mitigate the negative consequences of climate change.
Going from description of the diversity and disease associations of the human gut microbiota towards functional understanding and applications is challenging. In this Review, Raes and colleagues present synthetic ecology approaches that reduce the complexity and advance translation of human gut microbiota research.
Microbiome engineering has many potential applications, ranging from agriculture to medicine. In this Review, Lawson, McMahon and colleagues guide us through the design–build–test–learn cycle that has been successful in many disciplines and explain how it applies to microbiome engineering.
In this Review, Kolodziejczyk, Zheng and Elinav describe the latest advances in understanding diet–microbiota interactions, the individuality of gut microbiota composition and how this knowledge could be harnessed for personalized nutrition strategies to improve human health.
Simple animal models are emerging as valuable tools for microbiome research. In this Review, Douglas discusses the opportunity for microbiome research on the traditional biomedical models Drosophila melanogaster, Caenorhabditis elegans and zebrafish. Other systems, for example, hydra, squid and the honeybee, are valuable alternative models to address specific questions.
Perturbations in the intestinal microbiome are implicated in inflammatory bowel disease (IBD). In this Review, Xavier and colleagues highlight current knowledge of gut microbial factors linked to IBD pathogenesis and discuss how multiomics data from large-scale population studies in health and disease have been used to identify specific microbial strains, transcriptional changes and metabolic alterations associated with IBD.
Hydrothermal vents are unique habitats for chemosynthetic bacteria and archaea and the animals that live in symbiosis with them. In this Review, Dick explores the challenges and opportunities that vent ecosystems provide for microbial life and their relationship to biogeography.
Fungi are enormously diverse, not the least in potential genetic markers that can be used for high-throughput sequencing studies of the mycobiome. In this Review, Nilsson and colleagues provide advice for leveraging next-generation technologies to explore mycobiome diversity in different habitats.
The dynamic and polymicrobial oral microbiota is a direct precursor of diseases such as dental caries and periodontitis. In this Review, Lamont, Koo and Hajishengallis discuss the mechanisms by which oral microbial communities develop and become functionally specialized. They also examine the progression of polymicrobial communities towards pathogenicity.
In this Review, Gilbert and Stephens outline the history of the field of microbiology of the built environment and discuss insights into microbial ecology, adaptation and evolution. They consider the implications of this research, specifically, how it is changing the types of materials we use in buildings and how our built environments affect human health.
The microbiota can influence host behaviour through the gut–brain axis. In this Opinion, Johnson and Foster explore the evolution of this relationship and propose that adaptations of competing gut microorganisms may affect behaviour as a by‑product, leading to host dependence.
Culturomics was developed to culture and identify unknown bacteria that inhabit the human gut. In this Review, Raoult and colleagues discuss the development of culturomics and how it has extended our understanding of bacterial diversity, and highlight the potential implications for human health.
The first line of host defence against both encroaching commensal bacteria and invading enteric pathogens is the intestinal mucosal barrier, which is composed of epithelial cells and a host-secreted mucous layer. In this Review, Martens and colleagues discuss the complex interactions of commensal and pathogenic microorganisms with the intestinal mucosal barrier.
Complex microbial communities shape the dynamics of various environments. In this Review, Knight and colleagues discuss the best practices for performing a microbiome study, including experimental design, choice of molecular analysis technology, methods for data analysis and the integration of multiple omics data sets.
In this Opinion article, Banerjee et al. explore the importance of microbial keystone taxa and keystone guilds in microbiome structure and functioning, describe challenges in the characterization and manipulation of such taxa, and propose a definition of keystone taxa in microbial ecology.
Interactions among organisms are not limited to the exchange of electron donors. Most microorganisms are auxotrophs and thus rely on external nutrients for growth. In this Opinion article, Zengler and Zaramela postulate that auxotrophies and nutrient requirements among members of complex communities have profound implications for microbial interactions and thus the overall microbial network.
Our skin is home to millions of bacteria, fungi and viruses that comprise the skin microbiota. In this Review, Byrd and colleagues discuss recent insights into skin microbial communities, including their composition in health and disease, dynamics between species and interactions with the immune system.
In this Opinion article, Byndloss and Bäumler propose that host control over the microbial ecosystem in the large bowel is critical for the composition and function of its resident microbial organ, while disruption of host control triggers microbial organ dysfunction. This concept provides a theoretical framework for linking the gut microbiota to non-communicable diseases.
The interplay between nutrient intake, gut microbial metabolism and microorganism-driven engagement of host receptors contributes to the pathogenesis of cardiovascular disease. In this Review, Brown and Hazen discuss the gut microbial mechanisms that drive cardiovascular disease, with special emphasis on therapeutic interventions.
Soil contains a vast diversity of microorganisms that can directly or indirectly modulate soil processes and terrestrial ecosystems. In this Review, Fierer summarizes the challenges in characterizing the composition and functions of the soil microbiome, and discusses key future research directions.
The resilience of the microbiota can protect us from disease, but a resilient dysbiotic microbiota may also cause disease. This Opinion article discusses the concepts and mechanisms of microbial resilience against dietary, antibiotic or bacteriotherapy-induced perturbations and the implications these have for human health.
The transmission of commensal intestinal bacteria between humans could promote health by establishing, maintaining and replenishing microbial diversity in the microbiota of an individual. In this Review, Browne and colleagues discuss the mechanisms and factors that influence host-to-host transmission of the intestinal microbiota.
The microbiota influences the development of cancer and the effect of cancer therapies. In this Review, the authors summarize the interactions between the microbiota, the immune system and tumours and how manipulation of the microbiota can be used therapeutically.
The human gut is host to a dense microbial community that includes a large bacteriophage population. This Review summarizes bacteria and phage dynamics in health and disease, and considers how phages may be harnessed as novel therapeutics to improve disease outcomes.
The respiratory tract spans from the nostrils to the lung alveoli and these distinct niches host a diverse microbiota. In this Review, Man, de Steenhuijsen Piters and Bogaert discuss the role of the respiratory microbiota in the maintenance of human health.
The microbiota is central for host homeostasis and affects not only the gut but also other organs, including the lungs. In this Opinion article, Hansbro and colleagues explore the role of the microbiota in the gut–lung axis and lung disease.
Metagenome-wide association studies (MWAS) are designed to detect associations between the human microbiome and disease. In this Review, Jia and Wang describe the principal findings of MWAS of human diseases, and consider how these findings might be integrated into medical research and practice.
Molecular-based studies of fungal biodiversity have revealed fundamental differences from the biodiversity of bacteria, plants and animals. In this Review, Peay and colleagues consider the roles of ecology and fungal biology in determining fungal biodiversity at different spatial scales.
The gut of honey bees is inhabited by a small group of highly host-adapted bacteria. In this Review, Kwong and Moran detail the composition and functions of the microbiota of honey bees and highlight similarities and differences to the human microbiota.
In this Review, Turnbaugh and colleagues discuss several mechanisms by which the human gut microbiome affects the metabolism of xenobiotics, including drugs and dietary compounds, and explore how this knowledge can be applied to improve the treatment of human disease.
In this Progress article, Stephanie Karst describes how the gut microbiota promotes intestinal infection by enteric viruses. She discusses direct mechanisms by which bacteria stabilize viral particles and facilitate viral attachment to host cells, and indirect mechanisms by which the microbiota suppresses antiviral immune responses.
The gut microbiota has a strong impact on host physiology. In this Review, Mazmanian and colleagues describe the mechanisms that control the biogeography of bacteria in the gut and discuss the importance of the spatial localization of the gut microbiota during health and disease.
In this Opinion article, James Prosser considers the conceptual limitations of metagenomics and metatranscriptomics in contributing to our understanding of soil microbial ecology, and also explores potential opportunities for using these techniques to address specific ecological questions.
In this Review, Huttenhower and colleagues discuss how integrating multi-omic data types — including genomics, transcriptomics, proteomics and metabolomics — enables a better characterization of the composition and function of human-associated and environmental microbial communities.