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Almost there: transmission routes of bacterial symbionts between trophic levels.

Chiel E, Zchori-Fein E, Inbar M, Gottlieb Y, Adachi-Hagimori T, Kelly SE, Asplen MK, Hunter MS - PLoS ONE (2009)

Bottom Line: 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.In contrast with Rickettsia, Hamiltonella did not establish in any of the parasitoids tested, and none of the parasitoids acquired Hamiltonella by host feeding.

View Article: PubMed Central - PubMed

Affiliation: Department of Evolutionary and Environmental Biology, University of Haifa, Haifa, Israel. chiel@email.arizona.edu

ABSTRACT
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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A diagram illustrating the design of experiment 7, transmission of symbionts from B. tabaci to parasitoids, and 8, vertical transmission of symbionts in parasitoids.Infection status is indicated either by red “+” sign or blue “−” sign. R = Rickettsia, H = Hamiltonella. TRT = treatment. Whitefly hosts are illustrated as small yellow ovals on the (green) leaf disks. To test transmission of symbionts from B. tabaci to parasitoids, one female parasitoid was introduced to each leaf disk for 24 h, after which they were tested by PCR. From the emerging F1, one or two females from each replicate were used to continue to the vertical transmission experiment, while the rest of the cohort was tested by PCR (two-five from each cohort). The emerging F2 were all collected and two-five from each cohort were tested by PCR.
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pone-0004767-g001: A diagram illustrating the design of experiment 7, transmission of symbionts from B. tabaci to parasitoids, and 8, vertical transmission of symbionts in parasitoids.Infection status is indicated either by red “+” sign or blue “−” sign. R = Rickettsia, H = Hamiltonella. TRT = treatment. Whitefly hosts are illustrated as small yellow ovals on the (green) leaf disks. To test transmission of symbionts from B. tabaci to parasitoids, one female parasitoid was introduced to each leaf disk for 24 h, after which they were tested by PCR. From the emerging F1, one or two females from each replicate were used to continue to the vertical transmission experiment, while the rest of the cohort was tested by PCR (two-five from each cohort). The emerging F2 were all collected and two-five from each cohort were tested by PCR.

Mentions: There are three likely routes by which symbionts can be transmitted from the whitefly host to its parasitoids: 1) the parasitoid larva acquires symbionts while feeding and developing in an infected host; 2) the adult female wasps acquire symbionts via host-feeding (piercing of the whitefly integument with the ovipositor followed by consumption of host hemolymph); 3) adult wasps might acquire the symbiont via feeding on honeydew secretions of infected whitefly hosts. To test these pathways, cowpea leaf disks (30 mm diameter) infested with 30–50 R+ B. tabaci nymphs (2nd and 3rd instars) were placed on 1% agar inside 35 mm Petri dishes and sealed with screen lids. One male and one female of R− wasps (cured Er. emiratus and Er. eremicus grown for six generations on R− whiteflies or R− En. pergandiella directly from the culture) were introduced onto each leaf disk for 24 hrs and were then collected to 96% ethanol for PCR analysis. The percentage of infection status of these adults was used to determine the acquisition of the symbiont via either host-feeding or feeding on infected honeydew (scenarios 2 and 3 above). For controls, wasps from the same sources were introduced onto leaf disks bearing R− whiteflies, and some wasps were placed directly in ethanol, without exposure to hosts. The leaf disks bearing parasitized whiteflies were then incubated for approximately two weeks until wasp progeny emergence and then two to five (at least one male and one female) wasps from each disk were collected and placed in 96% ethanol. An estimate of the percentage of symbiont acquisition via exposure during development (scenario 1 above) was determined by the infection status of this second group of wasps. Results were subjected to a chi-square test (JMP 6.1 software, SAS Institute). Figure 1 illustrates the set up of this experiment, as well as the vertical transmission experiment (#8, below).


Almost there: transmission routes of bacterial symbionts between trophic levels.

Chiel E, Zchori-Fein E, Inbar M, Gottlieb Y, Adachi-Hagimori T, Kelly SE, Asplen MK, Hunter MS - PLoS ONE (2009)

A diagram illustrating the design of experiment 7, transmission of symbionts from B. tabaci to parasitoids, and 8, vertical transmission of symbionts in parasitoids.Infection status is indicated either by red “+” sign or blue “−” sign. R = Rickettsia, H = Hamiltonella. TRT = treatment. Whitefly hosts are illustrated as small yellow ovals on the (green) leaf disks. To test transmission of symbionts from B. tabaci to parasitoids, one female parasitoid was introduced to each leaf disk for 24 h, after which they were tested by PCR. From the emerging F1, one or two females from each replicate were used to continue to the vertical transmission experiment, while the rest of the cohort was tested by PCR (two-five from each cohort). The emerging F2 were all collected and two-five from each cohort were tested by PCR.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2651630&req=5

pone-0004767-g001: A diagram illustrating the design of experiment 7, transmission of symbionts from B. tabaci to parasitoids, and 8, vertical transmission of symbionts in parasitoids.Infection status is indicated either by red “+” sign or blue “−” sign. R = Rickettsia, H = Hamiltonella. TRT = treatment. Whitefly hosts are illustrated as small yellow ovals on the (green) leaf disks. To test transmission of symbionts from B. tabaci to parasitoids, one female parasitoid was introduced to each leaf disk for 24 h, after which they were tested by PCR. From the emerging F1, one or two females from each replicate were used to continue to the vertical transmission experiment, while the rest of the cohort was tested by PCR (two-five from each cohort). The emerging F2 were all collected and two-five from each cohort were tested by PCR.
Mentions: There are three likely routes by which symbionts can be transmitted from the whitefly host to its parasitoids: 1) the parasitoid larva acquires symbionts while feeding and developing in an infected host; 2) the adult female wasps acquire symbionts via host-feeding (piercing of the whitefly integument with the ovipositor followed by consumption of host hemolymph); 3) adult wasps might acquire the symbiont via feeding on honeydew secretions of infected whitefly hosts. To test these pathways, cowpea leaf disks (30 mm diameter) infested with 30–50 R+ B. tabaci nymphs (2nd and 3rd instars) were placed on 1% agar inside 35 mm Petri dishes and sealed with screen lids. One male and one female of R− wasps (cured Er. emiratus and Er. eremicus grown for six generations on R− whiteflies or R− En. pergandiella directly from the culture) were introduced onto each leaf disk for 24 hrs and were then collected to 96% ethanol for PCR analysis. The percentage of infection status of these adults was used to determine the acquisition of the symbiont via either host-feeding or feeding on infected honeydew (scenarios 2 and 3 above). For controls, wasps from the same sources were introduced onto leaf disks bearing R− whiteflies, and some wasps were placed directly in ethanol, without exposure to hosts. The leaf disks bearing parasitized whiteflies were then incubated for approximately two weeks until wasp progeny emergence and then two to five (at least one male and one female) wasps from each disk were collected and placed in 96% ethanol. An estimate of the percentage of symbiont acquisition via exposure during development (scenario 1 above) was determined by the infection status of this second group of wasps. Results were subjected to a chi-square test (JMP 6.1 software, SAS Institute). Figure 1 illustrates the set up of this experiment, as well as the vertical transmission experiment (#8, below).

Bottom Line: 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.In contrast with Rickettsia, Hamiltonella did not establish in any of the parasitoids tested, and none of the parasitoids acquired Hamiltonella by host feeding.

View Article: PubMed Central - PubMed

Affiliation: Department of Evolutionary and Environmental Biology, University of Haifa, Haifa, Israel. chiel@email.arizona.edu

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus