Evidence for Metabolic Provisioning by a Common Invertebrate Endosymbiont, Wolbachia pipientis, during Periods of Nutritional Stress

Wolbachia are ubiquitous inherited endosymbionts of invertebrates that invade host populations by modifying host reproductive systems. However, some strains lack the ability to impose reproductive modification and yet are still capable of successfully invading host populations. To explain this paradox, theory predicts that such strains should provide a fitness benefit, but to date none has been detected. Recently completed genome sequences of different Wolbachia strains show that these bacteria may have the genetic machinery to influence iron utilization of hosts. Here we show that Wolbachia infection can confer a positive fecundity benefit for Drosophila melanogaster reared on iron-restricted or -overloaded diets. Furthermore, iron levels measured from field-collected flies indicated that nutritional conditions in the field were overall comparable to those of flies reared in the laboratory on restricted diets. These data suggest that Wolbachia may play a previously unrecognized role as nutritional mutualists in insects

Increasing crop field size does not consistently exacerbate insect pest problems.

Increasing diversity on farms can enhance many key ecosystem services to and from agriculture, and natural control of arthropod pests is often presumed to be among them. The expectation that increasing the size of monocultural crop plantings exacerbates the impact of pests is common throughout the agroecological literature. However, the theoretical basis for this expectation is uncertain; mechanistic mathematical models suggest instead that increasing field size can have positive, negative, neutral, or even nonlinear effects on arthropod pest densities. Here, we report a broad survey of crop field-size effects: across 14 pest species, 5 crops, and 20,000 field years of observations, we quantify the impact of field size on pest densities, pesticide applications, and crop yield. We find no evidence that larger fields cause consistently worse pest impacts. The most common outcome (9 of 14 species) was for pest severity to be independent of field size; larger fields resulted in less severe pest problems for four species, and only one species exhibited the expected trend of larger fields worsening pest severity. Importantly, pest responses to field size strongly correlated with their responses to the fraction of the surrounding landscape planted to the focal crop, suggesting that shared ecological processes produce parallel responses to crop simplification across spatial scales. We conclude that the idea that larger field sizes consistently disrupt natural pest control services is without foundation in either the theoretical or empirical record

Comparative genomics suggests an independent origin of cytoplasmic incompatibility in Cardinium hertigii.

Terrestrial arthropods are commonly infected with maternally inherited bacterial symbionts that cause cytoplasmic incompatibility (CI). In CI, the outcome of crosses between symbiont-infected males and uninfected females is reproductive failure, increasing the relative fitness of infected females and leading to spread of the symbiont in the host population. CI symbionts have profound impacts on host genetic structure and ecology and may lead to speciation and the rapid evolution of sex determination systems. Cardinium hertigii, a member of the Bacteroidetes and symbiont of the parasitic wasp Encarsia pergandiella, is the only known bacterium other than the Alphaproteobacteria Wolbachia to cause CI. Here we report the genome sequence of Cardinium hertigii cEper1. Comparison with the genomes of CI-inducing Wolbachia pipientis strains wMel, wRi, and wPip provides a unique opportunity to pinpoint shared proteins mediating host cell interaction, including some candidate proteins for CI that have not previously been investigated. The genome of Cardinium lacks all major biosynthetic pathways but harbors a complete biotin biosynthesis pathway, suggesting a potential role for Cardinium in host nutrition. Cardinium lacks known protein secretion systems but encodes a putative phage-derived secretion system distantly related to the antifeeding prophage of the entomopathogen Serratia entomophila. Lastly, while Cardinium and Wolbachia genomes show only a functional overlap of proteins, they show no evidence of laterally transferred elements that would suggest common ancestry of CI in both lineages. Instead, comparative genomics suggests an independent evolution of CI in Cardinium and Wolbachia and provides a novel context for understanding the mechanistic basis of CI

Mean fecundity measures of female <i>D. melanogaster</i> reared on low iron food (tea).

<p>The total number of eggs laid by a single female was counted over a three-day period and the average calculated. Standard error bars are indicated; replicate numbers are noted within the columns. Uninfected females are denoted by an open bar, <i>Wolbachia</i>-infected females by a filled bar. Female flies reared on cornmeal fly diet are described as “Control.” Mean fecundities that are significantly different are denoted by * (p<0.05; ANOVA) or ** (p<0.001; Mann-Whitney U Test).</p

Mean fecundity measures of female <i>D. melanogaster</i> reared on high iron food (FeCl₃).

<p>The total number of eggs laid by a single female was counted over a three-day period and the average calculated. Standard error bars are indicated; replicate numbers are noted within the columns. Uninfected females are denoted by an open bar, <i>Wolbachia</i>-infected females by a filled bar. Female flies reared on cornmeal fly diet are described as “Control.” Mean fecundities that are significantly different are denoted by *(p<0.05) or ** (p<0.001; Mann-Whitney U Test).</p

Mean fecundity measures of female <i>D. melanogaster</i> reared on low iron food (BPS).

<p>The total number of eggs laid by a single female was counted over a three-day period and the average calculated. Standard error bars are indicated; replicate numbers are noted within the columns. Uninfected females are denoted by an open bar, <i>Wolbachia</i>-infected females by a filled bar. Female flies reared on cornmeal fly diet are described as “Control.” Mean fecundities that are significantly different are denoted by * (p<0.05; ANOVA).</p

General features of the genome of <i>Cardinium hertigii c</i>Eper1 and its closest sequenced relative <i>Amoebophilus asiaticus</i> 5a2.

<p>The genome sequence of <i>Cardinium</i> contains a single gap that could not be closed due to repetitive elements (*).</p

Metabolism, transport capabilities, and host cell interaction of <i>Cardinium hertigii c</i>Eper1.

<p>All predicted complete metabolic pathways and major transport proteins encoded on the genome are indicated. <i>Cardinium</i> lacks most biosynthetic pathways and imports nearly all essential metabolites from its host cell by employing a variety of transport proteins. Host cell interaction is mediated by secretion of effector proteins although no evidence for known protein secretion systems was found in the genome. A putative antifeeding prophage-derived secretion system could be used for translocation of proteins directly into the insect host cell by a contraction mechanism similar to type VI secretion systems <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003012#pgen.1003012-Basler1" target="_blank">[103]</a>.</p