Recurrent symbiont recruitment from fungal parasites in cicadas

Matsuura, Yu; Moriyama, Minoru; Łukasik, Piotr; Vanderpool, Dan; Tanahashi, Masahiko; Meng, Xian Ying; McCutcheon, John P.; Fukatsu, Takema

doi:10.1073/pnas.1803245115

Cited by 144 publications

(214 citation statements)

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“…Indeed, ancestral Coxiella ‐LE may have evolved overly reduced (degraded) genomes and become maladapted, opening the road to replacement by a new symbiont. This degeneration–replacement model has been proposed for other arthropods such as cicadas (Campbell et al, ; Łukasik et al, ; Matsuura et al, ), but replacements are expected to be transient making them difficult to observe (McCutcheon et al, ). In Amblyomma , the observations of three species with co‐infections by ancestral Coxiella ‐LE and recently acquired Francisella ‐LE may correspond to this transient state before extinction of Coxiella ‐LE.…”

Section: Discussionmentioning

confidence: 99%

“…This degeneration-replacement model has been proposed for other arthropods such as cicadas (Campbell et al, 2015;Łukasik et al, 2018;Matsuura et al, 2018) That ecological specialization to strict haematophagy is driven by nutritional symbiotic interactions is beyond doubt for ticks.…”

Section: Fl Ofmentioning

confidence: 91%

“…The functions of ancestral beneficial symbionts may be complemented by recently acquired cosymbionts and their coexistence can be ultimately stable over millions of years (Meseguer et al, 2017). New beneficial symbionts often originate from microbes that are abundant in the host environment, potentially including entomopathogens, parasites vectored by arthropods or other maternally inherited symbionts, primarily facultative (i.e., not essential) for host survival (Koga & Moran, 2014;Matsuura et al, 2018;McCutcheon et al, 2019;Sachs, Skophammer, & Regus, 2011). These facultative symbionts, however, determine important traits in arthropods: protection against natural enemies, adaptation to changing environments or reproductive traits (Engelstädter & Hurst, 2009;Ferrari & Vavre, 2011;Moran et al, 2008;Oliver et al, 2003).…”

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confidence: 99%

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Microbial community structure reveals instability of nutritional symbiosis during the evolutionary radiation of Amblyomma ticks

et al. 2020

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Mutualistic interactions with microbes have facilitated the adaptation of major eukaryotic lineages to restricted diet niches. Hence, ticks with their strictly blood‐feeding lifestyle are associated with intracellular bacterial symbionts through an essential B vitamin supplementation. In this study, examination of bacterial diversity in 25 tick species of the genus Amblyomma showed that three intracellular bacteria, Coxiella‐like endosymbionts (LE), Francisella‐LE and Rickettsia, are remarkably common. No other bacterium is as uniformly present in Amblyomma ticks. Almost all Amblyomma species were found to harbour a nutritive obligate symbiont, Coxiella‐LE or Francisella‐LE, that is able to synthesize B vitamins. However, despite the co‐evolved and obligate nature of these mutualistic interactions, the structure of microbiomes does not mirror the Amblyomma phylogeny, with a clear exclusion pattern between Coxiella‐LE and Francisella‐LE across tick species. Coxiella‐LE, but not Francisella‐LE, form evolutionarily stable associations with ticks, commonly leading to co‐cladogenesis. We further found evidence for symbiont replacements during the radiation of Amblyomma, with recent, and probably ongoing, invasions by Francisella‐LE and subsequent replacements of ancestral Coxiella‐LE through transient co‐infections. Nutritional symbiosis in Amblyomma ticks is thus not a stable evolutionary state, but instead arises from conflicting origins between unrelated but competing symbionts with similar metabolic capabilities.

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Section: Discussionmentioning

confidence: 99%

Section: Fl Ofmentioning

confidence: 91%

mentioning

confidence: 99%

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Microbial community structure reveals instability of nutritional symbiosis during the evolutionary radiation of Amblyomma ticks

et al. 2020

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“…Plant sap-feeding hemipteran insects usually harbour particular microbes essential for growth and reproduction of the host insects (Moran et al, 2005). Cicadas are known to have symbiotic bacteria and fungi, which are considered to supply nutrients in which xylem fluid is deficient, such as essential amino acids and vitamins (McCutcheon et al, 2009a, b;Christensen & Fogel, 2011;Matsuura et al, 2018). However, these symbiotic relationships have been shown to be vulnerable to high temperature caused by climate warming in some hemipteran insects (Prado et al, 2010;Kikuchi et al, 2016), as known in the famous example of coral bleaching (Baird et al, 2009;Ainsworth et al, 2016).…”

Section: Cicada Responses To Predicted Future Climate Changementioning

confidence: 99%

Ecophysiological responses to climate change in cicadas

Moriyama

Numata

2019

Physiol. Entomol.

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Cicadas are large hemipteran insects characterized by unique life‐history traits, such as extraordinarily long life cycles, a subterranean/terrestrial habitat transition, xylem sap‐feeding and melodious sound production. These fascinating features of cicadas have attracted much attention in the research fields of physiology and ecology, resulting in an accumulation of knowledge about the underlying mechanisms and their adaptive significance. Although community‐level responses to recent climate change have already been documented for cicada fauna, an understanding of their causal relationships is still at the initial stages. In this review, we summarize current knowledge about environmental adaptations of cicadas to facilitate a deeper understanding of the ecophysiological consequences of climate change. We first outline the diverse responses of cicadas to environmental factors, mainly temperature, and their strategies to cope with naturally fluctuating environments. Then, we discuss the consequence of upcoming climate change by consolidating the current findings. This review highlights the fact that fitness‐relevant activities are fine‐tuned to a species‐specific temperature optimum to achieve habitat segregation among coexisting species, implying that cicada diversity is highly susceptible to climate warming. As a result of their conspicuous large bodies and species‐specific calling songs, cicadas are promising candidates for use as bioindicator species to monitor ecological impacts of climate change. We encourage future works that continuously quantify population‐ and community‐level responses to upcoming climate change, as well as unveil mechanistic links between physiological traits and ecological consequences.

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“…Obligate symbiotic bacteria are pervasive among different groups of animals whose diets lack essential nutrients. These include blood- (Manzano-Marín et al, 2015;Smith et al, 2015;Říhová et al, 2017) and sap-feeders (xylem and phloem) (Husnik and McCutcheon, 2016;Matsuura et al, 2018;Santos-Garcia et al, 2014). Aphids (Hemiptera: Aphididae) are plant-sucking insects whose diet consists of plant phloem, which is poor in essential amino acids and B vitamins (Akman Gündüz and Douglas, 2009;Sandstrom and Moran, 1999;Ziegler, 1975).…”

Section: Introductionmentioning

confidence: 99%

Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems

Manzano-Marı́n

d’Acier

Clamens

et al. 2019

Preprint

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Many insects with a nutrient-restricted diet depend on obligate mutualistic bacteria for the provisioning of essential nutrients lacking from their food source, namely essential amino acids and B vitamins. Most aphids (Hemiptera: Aphididae), whose diet consists of phloem, rely on the bacterial endosymbiont Buchnera for the supply of the aforementioned compounds. However, in some aphid lineages Buchnera have lost the capability of producing these nutrients and thus the symbiotic consortium has accommodated an extra bacterial partner to supplement Buchnera's deficiencies. In this work, we explore the di-symbiotic nutritional endosymbiosis of a group of Cinara aphids which has been found to harbour both Buchnera and an Erwinia-related symbiont. Using fluorescence in situ hybridisation, we have located this symbiont to the bacteriome where it inhabits its own bacteriocytes. Through whole-genome sequencing of the endosymbionts of 9 species of Erwinia-associated Cinara aphids, we have found that Ewrinia genomes are highly syntenic and all show significant genome reduction. Additionally, Erwinia symbionts display phylogenetic congruency with Buchnera, suggesting long-term co-divergence. Most significantly, we found that not only is Erwinia capable of complementing Buchnera's auxotrophies, but that the genes involved in the biosynthesis of two B vitamins have actually been horizontally acquired from a Sodalis-related bacterium. Finally, this B-vitamin biosynthetic genes have been further transferred to a new Hamiltonella co-obligate symbiont in a specific Cinara lineage, thus displaying a tri-symbiotic system. These results highlight the important role horizontal gene transfer plays in the establishment of new obligate nutritional symbionts.

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Recurrent symbiont recruitment from fungal parasites in cicadas

Cited by 144 publications

References 89 publications

Microbial community structure reveals instability of nutritional symbiosis during the evolutionary radiation of Amblyomma ticks

Microbial community structure reveals instability of nutritional symbiosis during the evolutionary radiation of Amblyomma ticks

Ecophysiological responses to climate change in cicadas

Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems

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