Evolution of Microbiota–Host Associations: The Microbe’s Perspective
TL;DR: In this paper, the authors evaluate the key stages of the biphasic life cycle and propose a new conceptual framework for microbiota-host interactions which includes an integrative measure of microbial fitness, related to the parasite fitness parameter R0, and which will help in-depth assessment of these widespread associations.
About: This article is published in Trends in Microbiology.The article was published on 2021-03-02. It has received 19 citations till now.
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TL;DR: In this article, the authors analyzed 1358 genomes of Gut Microbes derived from host and environment-associated habitats and revealed host adaptation in gut Microbes is an evolutionary trade-off between transmission range and colonization abundance.
Abstract: Background Human-to-human transmission of symbiotic, anaerobic bacteria is a fundamental evolutionary adaptation essential for membership of the human gut microbiota. However, despite its importance, the genomic and biological adaptations underpinning symbiont transmission remain poorly understood. The Firmicutes are a dominant phylum within the intestinal microbiota that are capable of producing resistant endospores that maintain viability within the environment and germinate within the intestine to facilitate transmission. However, the impact of host transmission on the evolutionary and adaptive processes within the intestinal microbiota remains unknown. Results We analyze 1358 genomes of Firmicutes bacteria derived from host and environment-associated habitats. Characterization of genomes as spore-forming based on the presence of sporulation-predictive genes reveals multiple losses of sporulation in many distinct lineages. Loss of sporulation in gut Firmicutes is associated with features of host-adaptation such as genome reduction and specialized metabolic capabilities. Consistent with these data, analysis of 9966 gut metagenomes from adults around the world demonstrates that bacteria now incapable of sporulation are more abundant within individuals but less prevalent in the human population compared to spore-forming bacteria. Conclusions Our results suggest host adaptation in gut Firmicutes is an evolutionary trade-off between transmission range and colonization abundance. We reveal host transmission as an underappreciated process that shapes the evolution, assembly, and functions of gut Firmicutes.
15 citations
TL;DR: In this article, the authors investigate a simple model of a microbial lineage living, replicating, migrating and competing in and between two compartments: a host and an environment, and focus on the direction of selection at each point of the phenotypic space, defining an optimal way for the microbial lineage to increase its fitness.
Abstract: The concept of fitness is often reduced to a single component, such as the replication rate in a given habitat. For species with multi-step life cycles, this can be an unjustified oversimplification, as every step of the life cycle can contribute to the overall reproductive success in a specific way. In particular, this applies to microbes that spend part of their life cycles associated to a host. In this case, there is a selection pressure not only on the replication rates, but also on the phenotypic traits associated to migrating from the external environment to the host and vice-versa (i.e., the migration rates). Here, we investigate a simple model of a microbial lineage living, replicating, migrating and competing in and between two compartments: a host and an environment. We perform a sensitivity analysis on the overall growth rate to determine the selection gradient experienced by the microbial lineage. We focus on the direction of selection at each point of the phenotypic space, defining an optimal way for the microbial lineage to increase its fitness. We show that microbes can adapt to the two-compartment life cycle through either changes in replication or migration rates, depending on the initial values of the traits, the initial distribution across the two compartments, the intensity of competition, and the time scales involved in the life cycle versus the time scale of adaptation (which determines the adequate probing time to measure fitness). Overall, our model provides a conceptual framework to study the selection on microbes experiencing a host-associated life cycle.
11 citations
TL;DR: In this article , a review of the different aspects of AI-2, including its synthesis and its roles in the resistance to harsh environmental conditions, biofilm formation, adhesion and colonization, bacteriocin synthesis, and competition in LAB, are summarized.
Abstract: The LuxS/AI-2 quorum sensing system mediates interspecies and intraspecies signaling in bacteria and is associated with biofilm formation, pathogenicity, and resistance to harsh conditions. The regulatory mechanisms of the LuxS/AI-2 system in Vibrio harveyi, Escherichia coli, and Salmonella have been fully elucidated and have been termed lux operon and lsr operon. Furthermore, AI-2 is essential for the probiotic activities of lactic acid bacteria (LAB), including the gastrointestinal tract tolerance, adhesion, and colonization. However, there is limited information on the LuxS/AI-2 system in LAB. The health benefits of LAB regulated by AI-2 are emerging as a new research area in the field of probiotics, although the number of reports is limited. In this review, the different aspects of AI-2, including AI-2 synthesis and its roles in the resistance to harsh environmental conditions, biofilm formation, adhesion and colonization, bacteriocin synthesis, and competition in LAB, are summarized. AI-2 regulates the communication among LAB and their populations, thus influencing the probiotic activities of LAB. This review provides novel insights for the design of new, efficient, and specific probiotic products. However, the uncovering of the AI-2 regulatory pathways in LAB remains a critical challenge in the absence of AI-2 homologous proteins from of V. harveyi or E. coli.
5 citations
TL;DR: In this paper , the authors describe the establishment and manipulation of a synthetic insect-bacterial symbiosis in a weevil host and demonstrate that the symbiosis can be initiated in insects by the acquisition of environmental bacteria.
4 citations
TL;DR: Comparison of gut microbiota diversity and function among black-necked crane species revealed that unique bacteria are developed and acquired due to the selection pressure of high-altitude environments, indicating that altitude significantly impacted microbial communities’ composition and structure.
3 citations
References
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TL;DR: The fundamental role of the biofilm matrix is considered, describing how the characteristic features of biofilms — such as social cooperation, resource capture and enhanced survival of exposure to antimicrobials — all rely on the structural and functional properties of the matrix.
Abstract: Bacterial biofilms are formed by communities that are embedded in a self-produced matrix of extracellular polymeric substances (EPS). Importantly, bacteria in biofilms exhibit a set of 'emergent properties' that differ substantially from free-living bacterial cells. In this Review, we consider the fundamental role of the biofilm matrix in establishing the emergent properties of biofilms, describing how the characteristic features of biofilms - such as social cooperation, resource capture and enhanced survival of exposure to antimicrobials - all rely on the structural and functional properties of the matrix. Finally, we highlight the value of an ecological perspective in the study of the emergent properties of biofilms, which enables an appreciation of the ecological success of biofilms as habitat formers and, more generally, as a bacterial lifestyle.
3,277 citations
University of Wisconsin-Madison1, University of Hawaii2, University of Kiel3, Cornell University4, Max Planck Society5, Pasteur Institute6, Stanford University7, University of Helsinki8, University of Würzburg9, University of California, Berkeley10, University of New South Wales11, Harvard University12, California Institute of Technology13, University of Colorado Boulder14, University of Southern California15, University of North Carolina at Chapel Hill16, University of Connecticut17, Duke University18
TL;DR: Recent technological and intellectual advances that have changed thinking about five questions about how have bacteria facilitated the origin and evolution of animals; how do animals and bacteria affect each other’s genomes; how does normal animal development depend on bacterial partners; and how is homeostasis maintained between animals and their symbionts are highlighted.
Abstract: In the last two decades, the widespread application of genetic and genomic approaches has revealed a bacterial world astonishing in its ubiquity and diversity. This review examines how a growing knowledge of the vast range of animal–bacterial interactions, whether in shared ecosystems or intimate symbioses, is fundamentally altering our understanding of animal biology. Specifically, we highlight recent technological and intellectual advances that have changed our thinking about five questions: how have bacteria facilitated the origin and evolution of animals; how do animals and bacteria affect each other’s genomes; how does normal animal development depend on bacterial partners; how is homeostasis maintained between animals and their symbionts; and how can ecological approaches deepen our understanding of the multiple levels of animal–bacterial interaction. As answers to these fundamental questions emerge, all biologists will be challenged to broaden their appreciation of these interactions and to include investigations of the relationships between and among bacteria and their animal partners as we seek a better understanding of the natural world.
2,103 citations
TL;DR: Novel hypotheses for how nutrient selection, immune activation and other mechanisms control the biogeography of bacteria in the gut are considered, and the relevance of this spatial heterogeneity to health and disease is discussed.
Abstract: Animals assemble and maintain a diverse but host-specific gut microbial community. In addition to characteristic microbial compositions along the longitudinal axis of the intestines, discrete bacterial communities form in microhabitats, such as the gut lumen, colonic mucus layers and colonic crypts. In this Review, we examine how the spatial distribution of symbiotic bacteria among physical niches in the gut affects the development and maintenance of a resilient microbial ecosystem. We consider novel hypotheses for how nutrient selection, immune activation and other mechanisms control the biogeography of bacteria in the gut, and we discuss the relevance of this spatial heterogeneity to health and disease.
1,637 citations
TL;DR: Subjects sampled at varying time intervals exhibited individuality and temporal stability of SNP variation patterns, despite considerable composition changes of their gut microbiota, indicating that individual-specific strains are not easily replaced and that an individual might have a unique metagenomic genotype, which may be exploitable for personalized diet or drug intake.
Abstract: While large-scale efforts have rapidly advanced the understanding and practical impact of human genomic variation, the latter is largely unexplored in the human microbiome. We therefore developed a framework for metagenomic variation analysis and applied it to 252 fecal metagenomes of 207 individuals from Europe and North America. Using 7.4 billion reads aligned to 101 reference species, we detected 10.3 million single nucleotide polymorphisms (SNPs), 107,991 short indels, and 1,051 structural variants. The average ratio of non-synonymous to synonymous polymorphism rates of 0.11 was more variable between gut microbial species than across human hosts. Subjects sampled at varying time intervals exhibited individuality and temporal stability of SNP variation patterns, despite considerable composition changes of their gut microbiota. This implies that individual-specific strains are not easily replaced and that an individual might have a unique metagenomic genotype, which may be exploitable for personalized diet or drug intake.
771 citations
TL;DR: Priorities for future research include elucidation of microbial contributions to detoxification, especially of plant allelochemicals in phytophagous insects, and resistance to pathogens; as well as their role in among-insect communication; and the potential value of manipulation of the microbiota to control insect pests.
Abstract: All insects are colonized by microorganisms on the insect exoskeleton, in the gut and hemocoel, and within insect cells. The insect microbiota is generally different from microorganisms in the external environment, including ingested food. Specifically, certain microbial taxa are favored by the conditions and resources in the insect habitat, by their tolerance of insect immunity, and by specific mechanisms for their transmission. The resident microorganisms can promote insect fitness by contributing to nutrition, especially by providing essential amino acids, B vitamins, and, for fungal partners, sterols. Some microorganisms protect their insect hosts against pathogens, parasitoids, and other parasites by synthesizing specific toxins or modifying the insect immune system. Priorities for future research include elucidation of microbial contributions to detoxification, especially of plant allelochemicals in phytophagous insects, and resistance to pathogens; as well as their role in among-insect communicatio...
750 citations