Unfamiliar partnerships limit cnidarian holobiont acclimation to warming

Enhancing the resilience of corals to rising temperatures is now a matter of urgency, leading to growing efforts to explore the use of heat tolerant symbiont species to improve their thermal resilience. The notion that adaptive traits can be retained by transferring the symbionts alone, however, challenges the holobiont concept, a fundamental paradigm in coral research. Holobiont traits are products of a specific community (holobiont) and all its co‐evolutionary and local adaptations, which might limit the retention or transference of holobiont traits by exchanging only one partner. Here we evaluate how interchanging partners affect the short‐ and long‐term performance of holobionts under heat stress using clonal lineages of the cnidarian model system Aiptasia (host and Symbiodiniaceae strains) originating from distinct thermal environments. Our results show that holobionts from more thermally variable environments have higher plasticity to heat stress, but this resilience could not be transferred to other host genotypes through the exchange of symbionts. Importantly, our findings highlight the role of the host in determining holobiont productivity in response to thermal stress and indicate that local adaptations of holobionts will likely limit the efficacy of interchanging unfamiliar compartments to enhance thermal tolerance.     

Common and contrasting themes in host cell-targeted effectors from bacterial,fungal, oomycete and nematode plant symbionts described using the Gene Ontology

A wide diversity of plant-associated symbionts, including microbes, produce proteins that can enter host cells, or are injected into host cells in order to modify the physiology of the host to promote colonization. These molecules, termed effectors, commonly target the host defense signaling pathways in order to suppress the defense response. Others target the gene expression machinery or trigger specific modifications to host morphology or physiology that promote the nutrition and proliferation of the symbiont. When recognized by the host's surveillance machinery, which includes cognate resistance (R) gene products, defense responses are engaged to restrict pathogen proliferation. Effectors from diverse symbionts may be delivered into plant cells via varied mechanisms, including whole organism cellular entry (viruses, some bacteria and fungi), type III and IV secretion (in bacteria), physical injection (nematodes and insects) and protein translocation signal sequences (oomycetes and fungi). This mini-review will summarize both similarities and differences in effectors and effector delivery systems found in diverse plant-associated symbionts as well as how these are described with Plant-Associated Microbe Gene Ontology (PAMGO) terms.     

Colorado potato beetle manipulates plant defenses in local and systemic leaves

Herbivore microbial associates can affect diverse interactions between plants and insect herbivores. Some insect symbionts enable herbivores to expand host plant range or to facilitate host plant use by modifying plant physiology. However, little attention has been paid to the role of herbivore-associated microbes in manipulating plant defenses. We have recently shown that Colorado potato beetle secrete the symbiotic bacteria to suppress plant defenses. The bacteria in oral secretions from the beetle hijack defense signaling pathways of host plants and the suppression of induced plant defenses benefits the beetle’s performance. While the defense suppression by the beetle-associated bacteria has been investigated in local damaged leaves, little is known about the effects of the symbiotic bacteria on the manipulation of plant defenses in systemic undamaged leaves. Here, we demonstrate that the symbiotic bacteria suppress plant defenses in both local and systemic tissues when plants are attacked by antibiotic-untreated larvae.     

Interactions among multiple genomes: tsetse, its symbionts and trypanosomes

Insect-borne diseases exact a high public health burden and have a devastating impact on livestock and agriculture. To date, control has proved to be exceedingly difficult. One such disease that has plagued sub-Saharan Africa is caused by the protozoan African trypanosomes (Trypanosoma species) and transmitted by tsetse flies (Diptera: Glossinidae). This presentation describes the biology of the tsetse fly and its interactions with trypanosomes as well as its symbionts. Tsetse can harbor up to three distinct microbial symbionts, including two enterics (Wigglesworthia glossinidia and Sodalis glossinidius) as well as facultative Wolbachia infections, which influence host physiology. Recent investigations into the genome of the obligate symbiont Wigglesworthia have revealed characteristics indicative of its long co-evolutionary history with the tsetse host species. Comparative analysis of the commensal-like Sodalis with free-living enterics provides examples of adaptations to the host environment (physiology and ecology), reflecting genomic tailoring events during the process of transitioning into a symbiotic lifestyle. From an applied perspective, the extensive knowledge accumulated on the genomic and developmental biology of the symbionts coupled with our ability to both express foreign genes in these microbes in vitro and repopulate tsetse midguts with these engineered microbes now provides a means to interfere with the host physiological traits which contribute to vector competence promising a novel tool for disease management.     

Horizontal transfer of bacterial symbionts: heritability and fitness effects in a novel aphid host

Members of several bacterial lineages are known only as symbionts of insects and move among hosts through maternal transmission. Such vertical transfer promotes strong fidelity within these associations, favoring the evolution of microbially mediated effects that improve host fitness. However, phylogenetic evidence indicates occasional horizontal transfer among different insect species, suggesting that some microbial symbionts retain a generalized ability to infect multiple hosts. Here we examine the abilities of three vertically transmitted bacteria from the Gammaproteobacteria to infect and spread within a novel host species, the pea aphid, Acyrthosiphon pisum. Using microinjection, we transferred symbionts from three species of natural aphid hosts into a common host background, comparing transmission efficiencies between novel symbionts and those naturally infecting A. pisum. We also examined the fitness effects of two novel symbionts to determine whether they should persist under natural selection acting at the host level. Our results reveal that these heritable bacteria vary in their capacities to utilize A. pisum as a host. One of three novel symbionts failed to undergo efficient maternal transmission in A. pisum, and one of the two efficiently transmitted bacteria depressed aphid growth rates. Although these findings reveal that negative fitness effects and low transmission efficiency can prevent the establishment of a new infection following horizontal transmission, they also indicate that some symbionts can overcome these obstacles, accounting for their widespread distributions across aphids and related insects.     

Horizontal Transfer of Bacterial Symbionts: Heritability and Fitness Effects in a Novel Aphid Host

Members of several bacterial lineages are known only as symbionts of insects and move among hosts through maternal transmission. Such vertical transfer promotes strong fidelity within these associations, favoring the evolution of microbially mediated effects that improve host fitness. However, phylogenetic evidence indicates occasional horizontal transfer among different insect species, suggesting that some microbial symbionts retain a generalized ability to infect multiple hosts. Here we examine the abilities of three vertically transmitted bacteria from the Gammaproteobacteria to infect and spread within a novel host species, the pea aphid, Acyrthosiphon pisum. Using microinjection, we transferred symbionts from three species of natural aphid hosts into a common host background, comparing transmission efficiencies between novel symbionts and those naturally infecting A. pisum. We also examined the fitness effects of two novel symbionts to determine whether they should persist under natural selection acting at the host level. Our results reveal that these heritable bacteria vary in their capacities to utilize A. pisum as a host. One of three novel symbionts failed to undergo efficient maternal transmission in A. pisum, and one of the two efficiently transmitted bacteria depressed aphid growth rates. Although these findings reveal that negative fitness effects and low transmission efficiency can prevent the establishment of a new infection following horizontal transmission, they also indicate that some symbionts can overcome these obstacles, accounting for their widespread distributions across aphids and related insects.     

The role of host promiscuity in the invasion process of a seaweed holobiont

Invasive species are co-introduced with microbiota from their native range and also interact with microbiota found in the novel environment to which they are introduced. Host flexibility toward microbiota, or host promiscuity, is an important trait underlying terrestrial plant invasions. To test whether host promiscuity may be important in macroalgal invasions, we experimentally simulated an invasion in a common garden setting, using the widespread invasive macroalga Agarophyton vermiculophyllum as a model invasive seaweed holobiont. After disturbing the microbiota of individuals from native and non-native populations with antibiotics, we monitored the microbial succession trajectories in the presence of a new source of microbes. Microbial communities were strongly impacted by the treatment and changed compositionally and in terms of diversity but recovered functionally by the end of the experiment in most respects. Beta-diversity in disturbed holobionts strongly decreased, indicating that different populations configure more similar –or more common– microbial communities when exposed to the same conditions. This decline in beta-diversity occurred not only more rapidly, but was also more pronounced in non-native populations, while individuals from native populations retained communities more similar to those observed in the field. This study demonstrates that microbial communities of non-native A. vermiculophyllum are more flexibly adjusted to the environment and suggests that an intraspecific increase in host promiscuity has promoted the invasion process of A. vermiculophyllum. This phenomenon may be important among invasive macroalgal holobionts in general.Subject terms: Symbiosis, Molecular ecology, Microbial ecology     

Symbiosis as the way of eukaryotic life: The dependent co-origination of the body

Molecular analyses of symbiotic relationships are challenging our biological definitions of individuality and supplanting them with a new notion of normal part–whole relationships. This new notion is that of a ‘holobiont’, a consortium of organisms that becomes a functionally integrated ‘whole’. This holobiont includes the zoological organism (the ‘animal’) as well as its persistent microbial symbionts. This new individuality is seen on anatomical and physiological levels, where a diversity of symbionts form a new ‘organ system’ within the zoological organism and become integrated into its metabolism and development. Moreover, as in normal development, there are reciprocal interactions between the ‘host’ organism and its symbionts that alter gene expression in both sets of cells. The immune system, instead of being seen as functioning solely to keep microbes out of the body, is also found to develop, in part, in dialogue with symbionts. Moreover, the immune system is actively involved in the colonization of the zoological organism, functioning as a mechanism for integrating microbes into the animal-cell community. Symbionts have also been found to constitute a second mode of genetic inheritance, providing selectable genetic variation for natural selection. We develop, grow and evolve as multi-genomic consortia/teams/ecosystems.     

Can interspecies affairs in the dark lead to evolutionary innovation?

Evolutionary adaptation is the adjustment of species to a new or changing environment. Engaging in mutualistic microbial symbioses has been put forward as a key trait that promotes the differential, evolutionary success of many animal and plant lineages (McFall‐Ngai, 2008). Microbial mutualists allow these organisms to occupy new ecological niches where they could not have persisted on their own or would have been constrained by competitors. Vertical transmission of beneficial microbial symbionts from parents to the offspring is expected to link the adaptive association between a given host and microbe, and it can lead to coevolution and sometimes even cospeciation (Fisher, Henry, Cornwallis, Kiers, & West, 2017). Vertical transmission also causes bottlenecks that strongly reduce the effective population size and genetic diversity of the symbiont population. Moreover, vertically transmitted symbionts are assumed to have fewer opportunities to exchange genes with relatives in the environment. In a “From the Cover” article in this issue of Molecular Ecology, Breusing, Johnson, Vrijenhoek, and Young (2019) investigated whether hybridization among different host species could lead to interspecies exchange of otherwise strictly vertically transmitted symbionts. Hybridization of divergent lineages can potentially cause intrinsic and extrinsic incompatibilities, swamp rare alleles, and lead to population extinctions. In some cases, however, it might also create novel trait combinations that lead to evolutionary innovation (Marques, Meier, & Seehausen, 2019). Breusing et al. (2019) linked the concept of hybridization to symbiont transmission, and their findings have significant implications for the study of evolution of vertically transmitted symbionts and their hosts.     

Metabolic reconstruction of the near complete microbiome of the model sponge Ianthella basta

Many marine sponges host highly diverse microbiomes that contribute to various aspects of host health. Although the putative function of individual groups of sponge symbionts has been increasingly described, the extreme diversity has generally precluded in-depth characterization of entire microbiomes, including identification of syntrophic partnerships. The Indo-Pacific sponge Ianthella basta is emerging as a model organism for symbiosis research, hosting only three dominant symbionts: a Thaumarchaeotum, a Gammaproteobacterium, and an Alphaproteobacterium and a range of other low abundance or transitory taxa. Here, we retrieved metagenome assembled genomes (MAGs) representing >90% of I. basta's microbial community, facilitating the metabolic reconstruction of the sponge's near complete microbiome. Through this analysis, we identified metabolic complementarity between microbes, including vitamin sharing, described the importance of low abundance symbionts, and characterized a novel microbe–host attachment mechanism in the Alphaproteobacterium. We further identified putative viral sequences, highlighting the role viruses can play in maintaining symbioses in I. basta through the horizontal transfer of eukaryotic-like proteins, and complemented this data with metaproteomics to identify active metabolic pathways in bacteria, archaea, and viruses. This data provide the framework to adopt I. basta as a model organism for studying host–microbe interactions and provide a basis for in-depth physiological experiments.     

Metabolomics of reef benthic interactions reveals a bioactive lipid involved in coral defence

Holobionts are assemblages of microbial symbionts and their macrobial host. As extant representatives of some of the oldest macro-organisms, corals and algae are important for understanding how holobionts develop and interact with one another. Using untargeted metabolomics, we show that non-self interactions altered the coral metabolome more than self-interactions (i.e. different or same genus, respectively). Platelet activating factor (PAF) and Lyso-PAF, central inflammatory modulators in mammals, were major lipid components of the coral holobionts. When corals were damaged during competitive interactions with algae, PAF increased along with expression of the gene encoding Lyso-PAF acetyltransferase; the protein responsible for converting Lyso-PAF to PAF. This shows that self and non-self recognition among some of the oldest extant holobionts involve bioactive lipids identical to those in highly derived taxa like humans. This further strengthens the hypothesis that major players of the immune response evolved during the pre-Cambrian.     

The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems

Microbes are the unseen majority in soil and comprise a large portion of life's genetic diversity. Despite their abundance, the impact of soil microbes on ecosystem processes is still poorly understood. Here we explore the various roles that soil microbes play in terrestrial ecosystems with special emphasis on their contribution to plant productivity and diversity. Soil microbes are important regulators of plant productivity, especially in nutrient poor ecosystems where plant symbionts are responsible for the acquisition of limiting nutrients. Mycorrhizal fungi and nitrogen-fixing bacteria are responsible for c. 5–20% (grassland and savannah) to 80% (temperate and boreal forests) of all nitrogen, and up to 75% of phosphorus, that is acquired by plants annually. Free-living microbes also strongly regulate plant productivity, through the mineralization of, and competition for, nutrients that sustain plant productivity. Soil microbes, including microbial pathogens, are also important regulators of plant community dynamics and plant diversity, determining plant abundance and, in some cases, facilitating invasion by exotic plants. Conservative estimates suggest that c. 20 000 plant species are completely dependent on microbial symbionts for growth and survival pointing to the importance of soil microbes as regulators of plant species richness on Earth. Overall, this review shows that soil microbes must be considered as important drivers of plant diversity and productivity in terrestrial ecosystems.     

Persistence of bacterial pathogens as a physiological phenomenon

The complex ecosystem of humans and microbes has been presented as an associative symbiosis based on a mutual support of symbionts with different consequences for them. Conditions for the persistence of bacteria have been defined: their resistance to environmental factors, antagonism in biocenosis, and stability to withstand host defense mechanisms. The key role of bacterial peptidoglycan has been defined for their survival in an infected organism, and the classification for persistent mechanisms of pathogens has been given. The group of bacterial secreted protease providing microbial resistance to defense factors of the organism has been described. Host colonizing resistance has been presented as a physiological regulatory system controlling bacterial penetration into an organism. Regulatory mechanisms for bacterial persistence have been discussed.     

Coral reef invertebrate microbiomes correlate with the presence of photosymbionts

Coral reefs provide habitat for an array of marine invertebrates that host symbiotic microbiomes. Photosynthetic symbionts including Symbiodinium dinoflagellates and diatoms potentially influence the diversity of their host-associated microbiomes by releasing carbon-containing photosynthates and other organic compounds that fuel microbial metabolism. Here we used 16S ribosomal RNA (rRNA) gene amplicon pyrosequencing to characterise the microbiomes of 11 common Great Barrier Reef marine invertebrate species that host photosynthetic symbionts and five taxa in which they are absent. The presence of photosynthetic symbionts influenced the composition but not the species richness, evenness and phylogenetic diversity of invertebrate-associated microbiomes. Invertebrates without photosynthetic symbionts were dominated by Alphaproteobacteria, whereas those hosting photosynthetic symbionts were dominated by Gammaproteobacteria. Interestingly, many microbial species from photosymbiont-bearing invertebrates, including Oceanospirillales spp., Alteromonas spp., Pseudomonas spp., Halomonas spp., are implicated in the metabolism of dimethylsulfoniopropionate (DMSP). DMSP is produced in high concentrations by photosynthetic dinoflagellates and is involved in climate regulation by facilitating cloud formation. Microbiomes correlated with host taxa and replicate individuals from most sampled species grouped in distance-based redundancy analysis of retrieved 16S rRNA gene sequences. This study highlights the complex nature of invertebrate holobionts and confirms the importance of photosynthetic symbionts in structuring marine invertebrate bacterial communities.     

Rapid genotypic change and plasticity in arbuscular mycorrhizal fungi is caused by a host shift and enhanced by segregation

Arbuscular mycorrhizal fungi (AMF) are among the most abundant symbionts of plants, improving plant productivity and diversity. They are thought to mostly grow vegetatively, a trait assumed to limit adaptability. However, AMF can also harbor genetically different nuclei (nucleotypes). It has been shown that one AMF can produce genotypically novel offspring with proportions of different nucleotypes. We hypothesized that (1) AMF respond rapidly to a change of environment (plant host) through changes in the frequency of nucleotypes; (2) genotypically novel offspring exhibit different genetic responses to environmental change than the parent; and (3) genotypically novel offspring exhibit a wide range of phenotypic plasticity to a change of environment. We subjected AMF parents and offspring to a host shift. We observed rapid and large genotypic changes in all AMF lines that were not random. Genotypic and phenotypic responses were different among offspring and their parents. Even though growing vegetatively, AMF offspring display a broad range of genotypic and phenotypic changes in response to host shift. We conclude that AMF have the ability to rapidly produce variable progeny, increasing their probability to produce offspring with different fitness than their parents and, consequently, their potential adaptability to new environmental conditions. Such genotypic and phenotypic flexibility could be a fast alternative to sexual reproduction and is likely to be a key to the ecological success of AMF.     

The thrifty phenotype hypothesis: thrifty offspring or thrifty mother?

Medical research is increasingly focusing on the contribution of nutritional programming to disease in later life. Programming is a process whereby a stimulus during a critical window of time permanently affects subsequent structure, function or developmental schedule of the organism. The thrifty phenotype hypothesis is widely used to interpret such studies, with early growth restriction seen as adaptation to environmental deprivation. However, such permanent adjustment is less beneficial than maintaining flexibility so as to recover from early growth deficits if the environment improves. Thus, the existing thrifty phenotype hypothesis fails to explain why plasticity is lost so early in development in species with extended growth. One explanation is that the developing organism simply cannot maintain phenotypic plasticity throughout the period of organ growth. This article adds a life history perspective, arguing that programming of the offspring may in some species benefit maternal fitness more than it does that of individual offspring. Closing the critical window early in development allows the preservation of maternal strategy in offspring phenotype, which in humans benefits the mother by constraining offspring demand after weaning. The offspring gains by being buffered against environmental fluctuations during the most sensitive period of development, allowing coherent adaptation of organ growth to the state of the environment. The critical window is predicted to close when offspring physiology becomes independent of maternal physiology, the timing of which depends on offspring trait. Because placental nutrition and lactation buffer against short-term environmental fluctuations, maternal strategy is predicted to derive from long-term experience, encapsulated in maternal size and nutritional status. Such an approach implies that public health programmes for improving birth weight may be more effective if they target maternal development rather than nutrition during pregnancy. Equally, aggressive nutritional management of infants born small or pre-term may induce the very environmental fluctuations that are naturally softened by maternal nutrition.     

Safety and risk assessment for the human superorganism

This editorial on safety evaluation and risk assessment for the human superorganism introduces a series of papers arguing for a fundamental shift in how we approach human health risk assessment. In this series emphasis is placed on the risk of infectious disease. Our 21^stst century understanding of human biology is that, as holobionts, we possess a majority of microbial cells and genes. In fact, our microbes fundamentally affect our interactions with the external environment, metabolism, physiology, and risk of both pathology and disease. As holobionts, we require our microbial partners for us to be both complete and healthy. Using the 20^th century understanding of human biology, we failed to capture the effects of the microbiome in evaluating health risks. But 21^st century risk assessments such as those associated with exposure to specific microbial pathogens need to include the human microbiome. Microbiome status will be central in determining the health risks for both individuals and populations.     

Does host outcrossing disrupt compatibility with heritable symbionts?

Vertically transmitted microbes are common in macro‐organisms and can enhance host defense against environmental stress. Because vertical transmission couples host and symbiont lineages, symbionts may become specialized to host species or genotypes. Specialization and contrasting reproductive modes of symbiotic partners could create incompatibilities between inherited symbionts and novel host genotypes when hosts outcross or hybridize. Such incompatibilities could manifest as failed colonization or poor symbiont growth in host offspring that are genetically dissimilar from their maternal host. Moreover, outcrossing between host species could influence both host and symbiont reproductive performance. We tested these hypotheses by manipulating outcrossing between populations and species of two grasses, Elymus virginicus and E. canadensis, that host vertically transmitted fungal endophytes (genus Epichloё). In both greenhouse and field settings, we found that host–symbiont compatibility was robust to variation in host genetic background, spanning within‐population, between‐population and between‐species crosses. Symbiont transmission into the F₁ generation was generally high and weakly affected by host outcrossing. Furthermore, endophytes grew equally well in planta regardless of host genetic background and transmitted at high frequencies into the F₂ generation. However, outcrossing, especially inter‐specific hybridization, reduced reproductive fitness of the host, and thereby the symbiont. Our results challenge the hypothesis that host genetic recombination, which typically exceeds that of symbionts, is a disruptive force in heritable symbioses. Instead, symbionts may be sufficiently generalized to tolerate ecologically realistic variation in host outcrossing.     

Interwoven Biology of the Tsetse Holobiont

Microbial symbionts can be instrumental to the evolutionary success of their hosts. Here, we discuss medically significant tsetse flies (Diptera: Glossinidae), a group comprised of over 30 species, and their use as a valuable model system to study the evolution of the holobiont (i.e., the host and associated microbes). We first describe the tsetse microbiota, which, despite its simplicity, harbors a diverse range of associations. The maternally transmitted microbes consistently include two Gammaproteobacteria, the obligate mutualists Wigglesworthia spp. and the commensal Sodalis glossinidius, along with the parasitic Alphaproteobacteria Wolbachia. These associations differ in their establishment times, making them unique and distinct from previously characterized symbioses, where multiple microbial partners have associated with their host for a significant portion of its evolution. We then expand into discussing the functional roles and intracommunity dynamics within this holobiont, which enhances our understanding of tsetse biology to encompass the vital functions and interactions of the microbial community. Potential disturbances influencing the tsetse microbiome, including salivary gland hypertrophy virus and trypanosome infections, are highlighted. While previous studies have described evolutionary consequences of host association for symbionts, the initial steps facilitating their incorporation into a holobiont and integration of partner biology have only begun to be explored. Research on the tsetse holobiont will contribute to the understanding of how microbial metabolic integration and interdependency initially may develop within hosts, elucidating mechanisms driving adaptations leading to cooperation and coresidence within the microbial community. Lastly, increased knowledge of the tsetse holobiont may also contribute to generating novel African trypanosomiasis disease control strategies.