Interactions between insect vectors and plant pathogens span the parasitism-mutualism continuum.

Agricultural crops infected with vector-borne pathogens can suffer severe negative consequences, but the extent to which phytopathogens affect the fitness of their vector hosts remains unclear. Evolutionary theory predicts that selection on vector-borne pathogens will favour low virulence or mutualistic phenotypes in the vector, traits facilitating effective transmission between plant hosts. Here, we use a multivariate meta-analytic approach on 115 effect sizes across 34 unique plant-vector-pathogen systems to quantify the overall effect of phytopathogens on vector host fitness. In support of theoretical models, we report that phytopathogens overall have a neutral fitness effect on vector hosts. However, the range of fitness outcomes is diverse and span the parasitism-mutualism continuum. We found no evidence that various transmission strategies, or direct effects and indirect (plant-mediated) effects, of phytopathogens have divergent fitness outcomes for the vector. Our finding emphasizes diversity in tripartite interactions and the necessity for pathosystem-specific approaches to vector control.

Immune-mediated competition benefits protective microbes over pathogens in a novel host species.

Microbes that protect against infection inhabit hosts across the tree of life. It is unclear whether and how the host immune system may affect the formation of new protective symbioses. We investigated the transcriptomic response of Caenorhabditis elegans following novel interactions with a protective microbe (Enterococcus faecalis) able to defend against infection by pathogenic Staphylococcus aureus. We have previously shown that E. faecalis can directly limit pathogen growth within hosts. In this study, we show that colonisation by protective E. faecalis caused the differential expression of 1,557 genes in pathogen infected hosts, including the upregulation of immune genes such as lysozymes and C-type lectins. The most significantly upregulated host lysozyme gene, lys-7, impacted the competitive abilities of E. faecalis and S. aureus when knocked out. E. faecalis has an increased ability to resist lysozyme activity compared to S. aureus, suggesting that the protective microbe could gain a competitive advantage from this host response. Our finding that protective microbes can benefit from immune-mediated competition after introduction opens up new possibilities for biocontrol design and our understanding of symbiosis evolution. Crosstalk between the host immune response and microbe-mediated protection should favour the continued investment in host immunity and avoid the potentially risky evolution of host dependence.

Arsenophonus apicola sp. nov., isolated from the honeybee Apis mellifera.

The genus Arsenophonus has been traditionally considered to comprise heritable bacterial symbionts of arthropods. Recent work has reported a microbe related to the type species Arsenophonus nasoniae as infecting the honey bee, Apis mellifera. The association was unusual for members of the genus in that the microbe-host interaction arose through environmental and social exposure rather than vertical transmission. In this study, we describe the in vitro culture of ArsBeeUST, a strain of this microbe isolated from A. mellifera in the USA. The 16S rRNA sequence of the isolated strain indicates it falls within the genus Arsenophonus. Biolog analysis indicates the bacterium has a restricted range of nutrients that support growth. In vivo experiments demonstrate the strain proliferates rapidly on injection into A. mellifera hosts. We further report the closed genome sequence for the strain. The genome is 3.3 Mb and the G+C content is 37.6 mol%, which is smaller than A. nasoniae but larger than the genomes reported for non-culturable Arsenophonus symbionts. The genome is complex, with six extrachromosomal elements and 11 predicted intact phage elements, but notably less complex than A. nasoniae. Strain ArsBeeUST is clearly distinct from the type species A. nasoniae on the basis of genome sequence, with 92 % average nucleotide identity. Based on our results, we propose Arsenophonus apicola sp. nov., with the type strain ArsBeeUST (CECT 30499T=DSM113403T=LMG 32504T).

More or Less? The Effect of Symbiont Density in Protective Mutualisms.

AbstractSymbionts can provide hosts with effective protection from natural enemies, but it can sometimes come at a cost. It is unclear to what extent the density of symbionts modulates the cost and benefits of conferred protection. Here, we use a meta-analysis of 103 effect sizes from a broad taxonomic range of protective symbioses to show that the degree of both protection and cost afforded to hosts is a positive function of symbiont density. We found that the effects of symbiont density on protection and cost are robust across ecological contexts. Density-function relationships did not vary with host type, symbiont localization, or transmission mode, nor did they vary with the method of density manipulation. Taken together, our results suggest that symbiont density can be a key variable determining the costs and benefits of a protective interaction.

Reproductive consequences of transient pathogen exposure across host genotypes and generations.

To maximize fitness upon pathogenic infection, host organisms might reallocate energy and resources among life-history traits, such as reproduction and defense. The fitness costs of infection can result from both immune upregulation and direct pathogen exploitation. The extent to which these costs, separately and together, vary by host genotype and across generations is unknown. We attempted to disentangle these costs by transiently exposing wild isolates and a lab-domesticated strain of Caenorhabditis elegans nematodes to the pathogen Staphylococcus aureus, using exposure to heat-killed pathogens to distinguish costs due to immune upregulation and pathogen exploitation. We found that host nematodes exhibit a short-term delay in offspring production when exposed to live and heat-killed pathogen, but their lifetime fecundity (total offspring produced) recovered to control levels. We also found genetic variation between host isolates for both cumulative offspring production and magnitude of fitness costs. We further investigated whether there were maternal pathogen exposure costs (or benefits) to offspring and revealed a positive correlation between the magnitude of the pathogen-induced delay in the parent's first day of reproduction and the cost to offspring population growth. Our findings highlight the capacity for hosts to recover fecundity after transient exposure to a pathogen.

Transitions in symbiosis: evidence for environmental acquisition and social transmission within a clade of heritable symbionts.

A dynamic continuum exists from free-living environmental microbes to strict host-associated symbionts that are vertically inherited. However, knowledge of the forces that drive transitions in symbiotic lifestyle and transmission mode is lacking. Arsenophonus is a diverse clade of bacterial symbionts, comprising reproductive parasites to coevolving obligate mutualists, in which the predominant mode of transmission is vertical. We describe a symbiosis between a member of the genus Arsenophonus and the Western honey bee. The symbiont shares common genomic and predicted metabolic properties with the male-killing symbiont Arsenophonus nasoniae, however we present multiple lines of evidence that the bee Arsenophonus deviates from a heritable model of transmission. Field sampling uncovered spatial and seasonal dynamics in symbiont prevalence, and rapid infection loss events were observed in field colonies and laboratory individuals. Fluorescent in situ hybridisation showed Arsenophonus localised in the gut, and detection was rare in screens of early honey bee life stages. We directly show horizontal transmission of Arsenophonus between bees under varying social conditions. We conclude that honey bees acquire Arsenophonus through a combination of environmental exposure and social contacts. These findings uncover a key link in the Arsenophonus clades trajectory from free-living ancestral life to obligate mutualism, and provide a foundation for studying transitions in symbiotic lifestyle.

Microbial evolution and transitions along the parasite-mutualist continuum.

Virtually all plants and animals, including humans, are home to symbiotic microorganisms. Symbiotic interactions can be neutral, harmful or have beneficial effects on the host organism. However, growing evidence suggests that microbial symbionts can evolve rapidly, resulting in drastic transitions along the parasite-mutualist continuum. In this Review, we integrate theoretical and empirical findings to discuss the mechanisms underpinning these evolutionary shifts, as well as the ecological drivers and why some host-microorganism interactions may be stuck at the end of the continuum. In addition to having biomedical consequences, understanding the dynamic life of microorganisms reveals how symbioses can shape an organism's biology and the entire community, particularly in a changing world.

Microbiome: Evolution in a World of Interaction.

Ecological interactions can generate strong selection. Two new studies reveal that the tempo and patterns of evolutionary change in a mammalian gut commensal can be altered dramatically during interactions with both the host and its microbiome.

Identifying bacterial predictors of honey bee health.

Non-targeted approaches are useful tools to identify new or emerging issues in bee health. Here, we utilise next generation sequencing to highlight bacteria associated with healthy and unhealthy honey bee colonies, and then use targeted methods to screen a wider pool of colonies with known health status. Our results provide the first evidence that bacteria from the genus Arsenophonus are associated with poor health in honey bee colonies. We also discovered Lactobacillus and Leuconostoc spp. were associated with healthier honey bee colonies. Our results highlight the importance of understanding how the wider microbial population relates to honey bee colony health.