Almost There: Transmission Routes of Bacterial Symbionts between Trophic Levels

University of California, Berkeley, United States of America
PLoS ONE (Impact Factor: 3.23). 02/2009; 4(3):e4767. DOI: 10.1371/journal.pone.0004767
Source: PubMed


Many intracellular microbial symbionts of arthropods are strictly vertically transmitted and manipulate their host's reproduction in ways that enhance their own transmission. Rare horizontal transmission events are nonetheless necessary for symbiont spread to novel host lineages. Horizontal transmission has been mostly inferred from phylogenetic studies but the mechanisms of spread are still largely a mystery. Here, we investigated transmission of two distantly related bacterial symbionts--Rickettsia and Hamiltonella--from their host, the sweet potato whitefly, Bemisia tabaci, to three species of whitefly parasitoids: Eretmocerus emiratus, Eretmocerus eremicus and Encarsia pergandiella. We also examined the potential for vertical transmission of these whitefly symbionts between parasitoid generations. Using florescence in situ hybridization (FISH) and transmission electron microscopy we found that Rickettsia invades Eretmocerus larvae during development in a Rickettsia-infected host, persists in adults and in females, reaches the ovaries. However, Rickettsia does not appear to penetrate the oocytes, but instead is localized in the follicular epithelial cells only. Consequently, Rickettsia is not vertically transmitted in Eretmocerus wasps, a result supported by diagnostic polymerase chain reaction (PCR). In contrast, Rickettsia proved to be merely transient in the digestive tract of Encarsia and was excreted with the meconia before wasp pupation. Adults of all three parasitoid species frequently acquired Rickettsia via contact with infected whiteflies, most likely by feeding on the host hemolymph (host feeding), but the rate of infection declined sharply within a few days of wasps being removed from infected whiteflies. In contrast with Rickettsia, Hamiltonella did not establish in any of the parasitoids tested, and none of the parasitoids acquired Hamiltonella by host feeding. This study demonstrates potential routes and barriers to horizontal transmission of symbionts across trophic levels. The possible mechanisms that lead to the differences in transmission of species of symbionts among species of hosts are discussed.

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Available from: Elad Chiel
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    • "Interspecies horizontal transmission of endosymbionts is rare, and subsequent vertical transmission may be reduced in posterior generations of the infected population (Russell and Moran, 2005; Jaenike et al., 2007; Chiel et al., 2009). These transmissions may however be evolutionarily important if they contribute to endosymbiont fixation in the infected population (Chiel et al., 2009). The likely horizontal transmission of endosymbionts between maize and rice weevils and between the maize weevil and the parasitoid T. elegans is a potential experimental model to elucidate unanswered evolutionary questions pertaining the Sitophilus species and their adaptation to stored cereals. "
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    ABSTRACT: Grain weevils are hosts of two cellular endosymbionts: Wolbachia and “Sitophilus Primary Endosymbiont” (SPE). Wolbachia is a facultative endosymbiont, while SPE is an obligatory endosymbiont. Both Wolbachia and SPE are transmitted vertically, that is, from mother to offspring. There are circumstances in which transmission occurs among conspecific organisms or organisms of distinct species (horizontal transmission), and both vertical and horizontal transmissions play significant roles in shaping the host's ecology and evolution. We found molecular evidence for the horizontal transfer of Wolbachia between the maize weevil (Sitophilus zeamais Motschulsky) and the rice weevil (Sitophilus oryzae (L.)) and evidence of horizontal transfer of Wolbachia and SPE between the maize weevil and the parasitoid Theocolax elegans Westwood (Hymenoptera: Pteromalidae). Using 16S rRNA fragments of both symbionts, we verified the co-existence of two Wolbachia strains in maize weevil individuals from a Mexican population, one of which is typically from this species, while the other is from rice weevils. This finding provides evidence of the horizontal transmission of the endosymbiont between maize and rice weevil and supports the contention of similarity and relatedness between these weevil species. We also observed 100% similarity of 16S rRNA fragments between Wolbachia and SPE sequenced from the weevil parasitoid T. elegans and the maize weevil. This evidence suggests the horizontal transmission of both endosymbionts from the maize weevil to its parasitoid T. elegans. In addition to the importance of these findings for the ecology and evolution of weevils, the potential use of endosymbionts in innovative tactics of arthropod pest management in stored products also deserves attention and remains virtually unexplored.
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    • "To determine Rickettsia infection frequency in the population cage experiment, a chelex DNA extraction protocol was used (Chiel et al. 2009) and PCR amplification was conducted on single whitefly females. The PCR was conducted using Rickettsia-specific 16S rDNA primers (Chiel et al. 2009) and included a negative control of sterile water and a positive control of a Rickettsia-infected whitefly. PCR amplifications were carried out with a program used for Rickettsia diagnostic PCR in whiteflies (Himler et al. 2011). "
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    ABSTRACT: Inherited intracellular insect endosymbionts may manipulate host reproduction or provide fitness benefits to their hosts in ways that result in their rapid spread throughout a host population. Fitness benefits in particular can result in the increased pest potential of agriculturally important insects. While benefits due to endosymbiont infection have been well studied in laboratory assays, very little is known about how these benefits translate to insect performance in the field. Laboratory experiments have shown that the maternally inherited bacterial endosymbiont, Rickettsia, increases the fitness of its whitefly host, Bemisia tabaci, through improved fecundity, faster development times and female-biased sex ratios. We conducted field population cage studies to determine whether the benefits conferred by Rickettsia to whiteflies in the laboratory were evident on one of its major hosts, cotton, under field conditions in Arizona, USA. In cages with either Rickettsia-infected or uninfected whiteflies, we observed up to ten-fold higher whitefly egg and nymph densities when whiteflies were Rickettsia-infected compared with uninfected whiteflies throughout the season. We also observed a steep initial increase in Rickettsia frequency in population cages started with either 25% or 50% Rickettsia-infected whiteflies, with the 50% cages approaching fixation within three generations. Using growth rates obtained in the density cages, we calculated and compared an expected trajectory of the frequencies of Rickettsia infection with the observed frequencies. Results showed similar observed and expected frequencies of Rickettsia in the first two generations, followed by a significantly lower than expected frequency in three of four treatment/sample combinations at the end of the season. Taken together, these results confirm the patterns of fecundity and population growth observed in laboratory assays, under field conditions, as well as provides preliminary empirical support for a Rickettsia equilibrium frequency of less than 100%.
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    • "The presence of Wolbachia was determined using the Wolbachia-speciÞc 16S rDNA primers, V1 and V6 (OÕNeill et al. 1992). Screening for other B. tabaci symbionts was done using the primers and conditions described by Chiel et al. (2009). PCR products were visualized on 1.5% agarose gel using SYBR-Green (Cambrex Bio Science Rockland Inc.). "
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