Complex host/symbiont integration of a multi-partner symbiotic system in the eusocial aphid Ceratovacuna japonica

Yorimoto, Shunta; Hattori, Mitsuru; Kondo, Maki; Shigenobu, Shuji

doi:10.1016/j.isci.2022.105478

Cited by 14 publications

(21 citation statements)

References 108 publications

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“…symbiotica also occurs as a co-obligate nutritional symbiont in the related Chatosiphella genus. However, we show that Buchnera from the closely related Chaitophorus genus preserves an intact repertoire to synthesise all EAAs and B vitamins.Along the same line, very recently published evidence strongly suggests that members of the Ceratovacuna genus (Hormaphidinae: cerataphidini) relay on two nutritional symbionts, Buchnera and Arsenophonus (Yorimoto et al ., 2022). According to our analyses, representative from the other two tribes of Hormaphidinae, do not depend on additional symbionts from nutritional complementation.…”

Section: Discussionmentioning

confidence: 88%

“…symbiotica endosymbiont in Si. maydis (Renoz et al ., 2022b), and another one shows the evolution of a co-obligate symbiotic system in Ceratovacuna japonica (Hormaphidinae: Cerataphidini; Yorimoto et al ., 2022). These results, in light of the large-scale approach taken in this work, show that these multi-partner symbioses have evolved several times independently, even within subfamilies.…”

Section: Discussionmentioning

confidence: 99%

“…In fact, Bacteroidota 16S rRNA sequences were only found in two samples of Hormaphidinae aphids in our survey (Astegopteryx bambusae ACOE3753 and Reticulaphis mirabilis ACOE3769). Arsenophonus was found in many samples of Hormaphidinae, where it has been previously found to be common within this subfamily and, very recently, even found to be establishing a co-obligate association in Ceratovacuna japonica (Hormaphidinae: Cerataphidini; Yorimoto et al 2022). Aphidinae hosted many secondary symbionts, however, none appear to be fixed at least at the tribe or even genus level.…”

Section: Aphids Are Associated With a Large And Diverse Pool Of Secon...mentioning

confidence: 94%

“…Such co-obligate symbioses have indeed arose in at least two aphid groups: the Lachninae (Manzano-Marín et al ., 2017) and the Periphyllus genus (Chaitophorinae: Chaitophorini; Monnin et al ., 2020; Renoz et al ., 2022a). Very recently, an additional two reports of co-obligate symbioses have been published in two species from two different tribes: Sipha maydis (Chaitophorinae: Siphini; Renoz et al ., 2022b), which has been idenpendently analysed in the current work, and Ceratovacuna japonica (Hormaphidinae: Cerataphidini; Yorimoto et al ., 2022). These secondary co-obligate symbionts now complement evolved auxotrophies of their corresponding Buchnera partners, most commonly those for biotin and riboflavin and less often those for tryptophan and histidine.…”

Section: Introductionmentioning

confidence: 99%

“…Family names and counts are followed by the putative and known co-obligate symbiont taxa as inferred from the present study or previous genomic analysis studies. * Very recently published byYorimoto et al (2022)…”

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confidence: 99%

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Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineages

Manzano-Marı́n

d’Acier

Clamens

et al. 2022

Preprint

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Aphids are a large family of phloem-sap feeders. They typically rely on a single bacterial endosymbiont, Buchnera aphidicola, to supply them with essential nutrients lacking in their diet. This association with Buchnera was described in model aphid species from the Aphidinae subfamily and has been assumed to be representative of most aphids. However, in two lineages, Buchnera has lost some essential symbiotic functions and is now complemented by additional symbionts. Though these cases break our view of aphids harbouring a single obligate endosymbiont, we know little about the extent, nature, and evolution of these associations across aphid subfamilies. Here, using 16S rRNA amplicon sequencing on 223 aphid samples (147 species from 12 subfamilies) and metagenomics on 25 aphid species from nine subfamilies, we show that dual symbioses have evolved anew at least six times. We also show that these co-obligate symbionts have typically evolved from facultative symbiotic taxa. Genome-based metabolic inference confirms interdependencies between Buchnera and its partners for the production of essential nutrients but shows contributions vary across pairs of co-obligate associates. Lastly, fluorescent in situ hybridisation microscopy shows a common bacteriocyte localisation of newly acquired symbionts. Lastly, patterns of Buchnera genome evolution reveal that small genome reductions affecting a few key genes can be the onset of these dual systems, while large gene losses can occur without any co-obligate symbiont acquisition. Hence, the once thought exclusive Buchnera-aphid association appears fragile, with a few metabolic losses having recurrently promoted the establishment of a new co-obligate symbiotic partner.

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Section: Discussionmentioning

confidence: 88%

Section: Discussionmentioning

confidence: 99%

Section: Aphids Are Associated With a Large And Diverse Pool Of Secon...mentioning

confidence: 94%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

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Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineages

Manzano-Marı́n

d’Acier

Clamens

et al. 2022

Preprint

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Aphid adaptation in a changing environment through their bacterial endosymbionts: an overview, including a new major cereal pest (Rhopalosiphum maidis (Fitch) scenario

Csorba,

Dinescu,

Pircalabioru

et al. 2024

Symbiosis

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Aphids (Hemiptera: Aphididae) are small, phloem-feeding insects that exhibit remarkable adaptability and resilience to various environmental conditions, including heat stress. Recent research has shed light on the role of bacterial symbionts in influencing the heat tolerance of aphids. Additionally, an intriguing avenue of investigation has explored how aphids can acquire bacterial symbionts through a unique mechanism involving soil nematodes. In this paper, we provide an in-depth overview of the interplay between heat stress, bacterial symbionts, and soil nematodes in the context of aphid biology. In reviewing the existing literature and collating available knowledge, we highlight the mechanisms by which bacterial symbionts contribute to aphid heat stress tolerance and examine the symbiont acquisition process facilitated by soil nematodes. Furthermore, we discuss the implications of these symbiotic associations in relation to the ecology, evolution, and agricultural management of a major globally expanding pest aphid, the corn leaf aphid, Rhopalosiphum maidis (Fitch). Overall, it may be concluded that both primary and secondary bacterial endosymbionts play a significant role in aphid biology with evolutionary consequences. These include adaptations through bacterial symbionts in terms of longevity and fecundity, heat shock tolerance, and resistance to fungal pathogens and primary hymenopterous wasp parasitoids.

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Social aphids: emerging model for studying insect sociality

Zhang,

Liu,

Huang

2024

Current Opinion in Insect Science

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Complex host/symbiont integration of a multi-partner symbiotic system in the eusocial aphid Ceratovacuna japonica

Cited by 14 publications

References 108 publications

Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineages

Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineages

Aphid adaptation in a changing environment through their bacterial endosymbionts: an overview, including a new major cereal pest (Rhopalosiphum maidis (Fitch) scenario

Social aphids: emerging model for studying insect sociality

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