Abstract
Insect guts present distinctive environments for microbial colonization, and bacteria in the gut potentially provide many beneficial services to their hosts. Insects display a wide range in ...degree of dependence on gut bacteria for basic functions. Most insect guts contain relatively few microbial species as compared to mammalian guts, but some insects harbor large gut communities of specialized bacteria. Others are colonized only opportunistically and sparsely by bacteria common in other environments. Insect digestive tracts vary extensively in morphology and physicochemical properties, factors that greatly influence microbial community structure. One obstacle to the evolution of intimate associations with gut microorganisms is the lack of dependable transmission routes between host individuals. Here, social insects, such as termites, ants, and bees, are exceptions: social interactions provide opportunities for transfer of gut bacteria, and some of the most distinctive and consistent gut communities, with specialized beneficial functions in nutrition and protection, have been found in social insect species. Still, gut bacteria of other insects have also been shown to contribute to nutrition, protection from parasites and pathogens, modulation of immune responses, and communication. The extent of these roles is still unclear and awaits further studies.
Different insect groups are host to a broad diversity of gut microbial communities, which vary in complexity, extent of adaptation to the host gut environment, and roles in host ecology and function.
Gut microbiomes play crucial roles in animal health, and shifts in the gut microbial community structure can have detrimental impacts on hosts. Studies with vertebrate models and human subjects ...suggest that antibiotic treatments greatly perturb the native gut community, thereby facilitating proliferation of pathogens. In fact, persistent infections following antibiotic treatment are a major medical issue. In apiculture, antibiotics are frequently used to prevent bacterial infections of larval bees, but the impact of antibiotic-induced dysbiosis (microbial imbalance) on bee health and susceptibility to disease has not been fully elucidated. Here, we evaluated the effects of antibiotic exposure on the size and composition of honeybee gut communities. We monitored the survivorship of bees following antibiotic treatment in order to determine if dysbiosis of the gut microbiome impacts honeybee health, and we performed experiments to determine whether antibiotic exposure increases susceptibility to infection by opportunistic pathogens. Our results show that antibiotic treatment can have persistent effects on both the size and composition of the honeybee gut microbiome. Antibiotic exposure resulted in decreased survivorship, both in the hive and in laboratory experiments in which bees were exposed to opportunistic bacterial pathogens. Together, these results suggest that dysbiosis resulting from antibiotic exposure affects bee health, in part due to increased susceptibility to ubiquitous opportunistic pathogens. Not only do our results highlight the importance of the gut microbiome in honeybee health, but they also provide insights into how antibiotic treatment affects microbial communities and host health.
Animals are distinguished by having guts-organs that must extract nutrients from food yet also bar invasion by pathogens. Most guts are colonized by nonpathogenic microorganisms, but the functions of ...these microbes, or even the reasons why they occur in the gut, vary widely among animals. Sometimes these microorganisms have codiversified with hosts; sometimes they live mostly elsewhere in the environment. Either way, gut microorganisms often benefit hosts. Benefits may reflect evolutionary addiction, whereby hosts incorporate gut microorganisms into normal developmental processes. But benefits often include novel ecological capabilities; for example, many metazoan clades exist by virtue of gut communities enabling new dietary niches. Animals vary immensely in their dependence on gut microorganisms, from lacking them entirely to using them as food or to obligate dependence for development, nutrition, or protection. Many consequences of gut microorganisms for hosts can be ascribed to microbial community processes and the host's ability to shape these processes.
Glyphosate perturbs the gut microbiota of honey bees Motta, Erick V. S.; Raymann, Kasie; Moran, Nancy A.
Proceedings of the National Academy of Sciences - PNAS,
10/2018, Letnik:
115, Številka:
41
Journal Article
Recenzirano
Odprti dostop
Glyphosate, the primary herbicide used globally for weed control, targets the 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) enzyme in the shikimate pathway found in plants and some ...microorganisms. Thus, glyphosate may affect bacterial symbionts of animals living near agricultural sites, including pollinators such as bees. The honey bee gut microbiota is dominated by eight bacterial species that promote weight gain and reduce pathogen susceptibility. The gene encoding EPSPS is present in almost all sequenced genomes of bee gut bacteria, indicating that they are potentially susceptible to glyphosate. We demonstrated that the relative and absolute abundances of dominant gut microbiota species are decreased in bees exposed to glyphosate at concentrations documented in the environment. Glyphosate exposure of young workers increased mortality of bees subsequently exposed to the opportunistic pathogen Serratia marcescens. Members of the bee gut microbiota varied in susceptibility to glyphosate, largely corresponding to whether they possessed an EPSPS of class I (sensitive to glyphosate) or class II (insensitive to glyphosate). This basis for differences in sensitivity was confirmed using in vitro experiments in which the EPSPS gene from bee gut bacteria was cloned into Escherichia coli. All strains of the core bee gut species, Snodgrassella alvi, encode a sensitive class I EPSPS, and reduction in S. alvi levels was a consistent experimental result. However, some S. alvi strains appear to possess an alternative mechanism of glyphosate resistance. Thus, exposure of bees to glyphosate can perturb their beneficial gut microbiota, potentially affecting bee health and their effectiveness as pollinators.
Many eukaryotes have obligate associations with microorganisms that are transmitted directly between generations. A model for heritable symbiosis is the association of aphids, a clade of sap-feeding ...insects, and Buchnera aphidicola , a gammaproteobacterium that colonized an aphid ancestor 150 million years ago and persists in almost all 5,000 aphid species. Symbiont acquisition enables evolutionary and ecological expansion; aphids are one of many insect groups that would not exist without heritable symbiosis. Receiving less attention are potential negative ramifications of symbiotic alliances. In the short run, symbionts impose metabolic costs. Over evolutionary time, hosts evolve dependence beyond the original benefits of the symbiosis. Symbiotic partners enter into an evolutionary spiral that leads to irreversible codependence and associated risks. Host adaptations to symbiosis (e.g., immune-system modification) may impose vulnerabilities. Symbiont genomes also continuously accumulate deleterious mutations, limiting their beneficial contributions and environmental tolerance. Finally, the fitness interests of obligate heritable symbionts are distinct from those of their hosts, leading to selfish tendencies. Thus, genes underlying the hostâsymbiont interface are predicted to follow a coevolutionary arms race, as observed for genes governing hostâpathogen interactions. On the macroevolutionary scale, the rapid evolution of interacting symbiont and host genes is predicted to accelerate host speciation rates by generating genetic incompatibilities. However, degeneration of symbiont genomes may ultimately limit the ecological range of host species, potentially increasing extinction risk. Recent results for the aphidâ Buchnera symbiosis and related systems illustrate that, whereas heritable symbiosis can expand ecological range and spur diversification, it also presents potential perils.
•The honey bee gut microbiome contains five core bacterial species mainly in hindguts.•This core microbiome is implicated in nutrition and development of adult workers.•Bee guts often contain low ...numbers of potential pathogens such as Serratia species.•Gut dysbiosis is associated with pathogen invasion and higher mortality.•Antibiotics disrupt the healthy microbiome, and may elevate disease susceptibility.
The role of the gut microbiome in animal health has become increasingly evident. Unlike most other insects, honey bees possess a highly conserved and specialized core gut microbiome, which consists of nine bacterial species and is acquired mostly through social transmission. Five of these species are ubiquitous in honey bees and are also present in bumble bees. Recent studies have shown that the bee gut microbiome plays a role in metabolism, immune function, growth and development, and protection against pathogens. Disruption of the gut microbiome has also been shown to have detrimental effects on bee health. Overall, evidence suggests that the gut microbiome plays an important role in bee health and disease.
With the increasing appreciation for the crucial roles that microbial symbionts play in the development and fitness of plant and animal hosts, there has been a recent push to interpret evolution ...through the lens of the "hologenome"--the collective genomic content of a host and its microbiome. But how symbionts evolve and, particularly, whether they undergo natural selection to benefit hosts are complex issues that are associated with several misconceptions about evolutionary processes in host-associated microbial communities. Microorganisms can have intimate, ancient, and/or mutualistic associations with hosts without having undergone natural selection to benefit hosts. Likewise, observing host-specific microbial community composition or greater community similarity among more closely related hosts does not imply that symbionts have coevolved with hosts, let alone that they have evolved for the benefit of the host. Although selection at the level of the symbiotic community, or hologenome, occurs in some cases, it should not be accepted as the null hypothesis for explaining features of host-symbiont associations.
Herbivory, defined as feeding on live plant tissues, is characteristic of highly successful and diverse groups of insects and represents an evolutionarily derived mode of feeding. Plants present ...various nutritional and defensive barriers against herbivory; nevertheless, insects have evolved a diverse array of mechanisms that enable them to feed and develop on live plant tissues. For decades, it has been suggested that insect‐associated microbes may facilitate host plant use, and new molecular methodologies offer the possibility to elucidate such roles. Based on genomic data, specialized feeding on phloem and xylem sap is highly dependent on nutrient provisioning by intracellular symbionts, as exemplified by Buchnera in aphids, although it is unclear whether such symbionts play a substantive role in host plant specificity of their hosts. Microorganisms present in the gut or outside the insect body could provide more functions including digestion of plant polymers and detoxification of plant‐produced toxins. However, the extent of such contributions to insect herbivory remains unclear. We propose that the potential functions of microbial symbionts in facilitating or restricting the use of host plants are constrained by their location (intracellular, gut or environmental), and by the fidelity of their associations with insect host lineages. Studies in the next decade, using molecular methods from environmental microbiology and genomics, will provide a more comprehensive picture of the role of microbial symbionts in insect herbivory.
The recent discovery that the human and other mammalian genomes produce thousands of long non-coding RNAs (lncRNAs) raises many fascinating questions. These mRNA-like molecules, which lack ...significant protein-coding capacity, have been implicated in a wide range of biological functions through diverse and as yet poorly understood molecular mechanisms. Despite some recent insights into how lncRNAs function in such diverse cellular processes as regulation of gene expression and assembly of cellular structures, by and large, the key questions regarding lncRNA mechanisms remain to be answered. In this review, we discuss recent advances in understanding the biology of lncRNAs and propose avenues of investigation that may lead to fundamental new insights into their functions and mechanisms of action. Finally, as numerous lncRNAs are dysregulated in human diseases and disorders, we also discuss potential roles for these molecules in human health.
Many animals depend on microbial symbionts to provide nutrition, defence or other services. Holometabolous insects, as well as other animals that undergo metamorphosis, face unique constraints on ...symbiont maintenance. Microbes present in larvae encounter a radical transformation of their habitat and may also need to withstand chemical and immunological challenges. Metamorphosis also provides an opportunity, in that symbiotic associations can be decoupled over development. For example, some holometabolous insects maintain the same symbiont as larvae and adults, but house it in different tissues; in other species, larvae and adults may harbour entirely different types or numbers of microbes, in accordance with shifts in host diet or habitat. Such flexibility may provide an advantage over hemimetabolous insects, in which selection on adult-stage microbial associations may be constrained by its negative effects on immature stages, and vice versa. Additionally, metamorphosis itself can be directly influenced by symbionts. Across disparate insect taxa, microbes protect hosts from pathogen infection, supply nutrients essential for rebuilding the adult body and provide cues regulating pupation. However, microbial associations remain completely unstudied for many families and even orders of Holometabola, and future research will undoubtedly reveal more links between metamorphosis and microbiota, two widespread features of animal life. This article is part of the theme issue 'The evolution of complete metamorphosis'.
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