Transovarial Transmission of Symbionts in Insects

Szklarzewicz, Teresa; Michalik, Anna

doi:10.1007/978-3-319-60855-6_3

Cited by 45 publications

(49 citation statements)

References 93 publications

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“…4 ). More generally, at this resolution, the mode of symbiont transmission appears well conserved throughout auchenorrhynchan insects ( 18 , 34 ). In mature cicada females, Hodgkinia and Sulcia cells are released from separate regions of the bacteriome into the hemolymph ( Fig.…”

Section: Resultsmentioning

confidence: 98%

Changes in Endosymbiont Complexity Drive Host-Level Compensatory Adaptations in Cicadas

Campbell

Łukasik

Meyer

et al. 2018

mBio

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Sap-feeding insects critically rely on one or more bacteria or fungi to provide essential nutrients that are not available at sufficient levels in their diets. These microbes are passed between insect generations when the mother places a small packet of microbes into each of her eggs before it is laid. We have previously described an unusual lineage fragmentation process in a nutritional endosymbiotic bacterium of cicadas called Hodgkinia. In some cicadas, a single Hodgkinia lineage has split into numerous related lineages, each performing a subset of original function and therefore each required for normal host function. Here we test how this splitting process affects symbiont transmission to eggs. We find that cicadas dramatically increase the titer of Hodgkinia cells passed to each egg in response to lineage fragmentation, and we hypothesize that this increase in bacterial cell count is one of the major costs associated with endosymbiont fragmentation.

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Section: Resultsmentioning

confidence: 98%

Changes in Endosymbiont Complexity Drive Host-Level Compensatory Adaptations in Cicadas

Campbell

Łukasik

Meyer

et al. 2018

mBio

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“…4). More generally, at this resolution, the mode of symbiont transmission appears well conserved throughout auchenorrhynchan insects (16,37). In mature cicada females, Hodgkinia and Sulcia cells are released from separate regions of the bacteriome into the hemolymph (Fig.…”

Section: Resultsmentioning

confidence: 93%

Changes in endosymbiont complexity drive host-level compensatory adaptations in cicadas

Campbell

Łukasik

Meyer

et al. 2018

Preprint

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For insects that depend on one or more bacterial endosymbionts for survival, it is critical that these bacteria are faithfully transmitted between insect generations. Cicadas harbor two essential bacterial endosymbionts, Sulcia muelleri and Hodgkinia cicadicola. In some cicada species, Hodgkinia has fragmented into multiple distinct cellular and genomic lineages that can differ in abundance by more than two orders of magnitude. This complexity presents a potential problem for the host cicada, because low-abundance-but-essential Hodgkinia lineages risk being lost during the symbiont transmission bottleneck from mother to egg. Here we show that all cicada eggs seem to receive the full complement of Hodgkinia lineages, and that in cicadas with more complex Hodgkinia this outcome is achieved by increasing the number of Hodgkinia cells transmitted by up to six-fold. We further show that cicada species with varying Hodgkinia complexity do not visibly alter their transmission mechanism at the resolution of cell biological structures. Together these data suggest that a major cicada adaptation to changes in endosymbiont complexity is an increase in the number of Hodgkinia cells transmitted to each egg. We hypothesize that the requirement to increase the symbiont titer is one of the costs associated with Hodgkinia fragmentation.

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“…It should be noted that besides the eriococcid species which have been examined so far, infection at the anterior pole of the oocyte has been observed in pseudococcids (von Dohlen et al, 2001) and putoids (Szklarzewicz et al, 2018). In auchenorrhynchans, aphids, whiteflies, psyllids and most species of scale insects symbionts migrate to the oocyte through the follicular epithelium surrounding the posterior pole of the oocyte (reviewed in Buchner, 1965;Szklarzewicz and Michalik, 2017).…”

Section: Discussionmentioning

confidence: 99%

Coexistence of novel gammaproteobacterial and Arsenophonus symbionts in the scale insect Greenisca brachypodii (Hemiptera, Coccomorpha: Eriococcidae)

Michalik

Schulz

Michalik

et al. 2018

Environmental Microbiology

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Scale insects are commonly associated with obligate, intracellular microorganisms which play important roles in complementing their hosts with essential nutrients. Here we characterized the symbiotic system of Greenisca brachypodii, a member of the family Eriococcidae. Histological and ultrastructural analyses have indicated that G. brachypodii is stably associated with coccoid and rod-shaped bacteria. Phylogenetic analyses have revealed that the coccoid bacteria represent a sister group to the secondary symbiont of the mealybug Melanococcus albizziae, whereas the rod-shaped symbionts are close relatives of Arsenophonus symbionts in insects - to our knowledge, this is the first report of the presence of Arsenophonus bacterium in scale insects. As a comparison of 16S and 23S rRNA genes sequences of the G. brachypodii coccoid symbiont with other gammaprotebacterial sequences showed only low similarity (∼90%), we propose the name 'Candidatus Kotejella greeniscae' for its tentative classification. Both symbionts are transovarially transmitted from one generation to the next. The infection takes place in the neck region of the ovariole. The bacteria migrate between follicular cells, as well as through the cytoplasm of those cells to the perivitelline space, where they form a characteristic 'symbiont ball'. Our findings provide evidence for a polyphyletic origin of symbionts of Eriococcidae.

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Transovarial Transmission of Symbionts in Insects

Cited by 45 publications

References 93 publications

Changes in Endosymbiont Complexity Drive Host-Level Compensatory Adaptations in Cicadas

Changes in Endosymbiont Complexity Drive Host-Level Compensatory Adaptations in Cicadas

Changes in endosymbiont complexity drive host-level compensatory adaptations in cicadas

Coexistence of novel gammaproteobacterial and Arsenophonus symbionts in the scale insect Greenisca brachypodii (Hemiptera, Coccomorpha: Eriococcidae)

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