Symbiont Digestive Range Reflects Host Plant Breadth in Herbivorous Beetles

Salem, Hassan; Kirsch, Roy; Pauchet, Yannick; Berasategui, Aileen; Fukumori, Kayoko; Moriyama, Minoru; Cripps, Michael G.; Windsor, Donald M.; Fukatsu, Takema; Gerardo, Nicole M.

doi:10.1016/j.cub.2020.05.043

Cited by 69 publications

(88 citation statements)

References 90 publications

(149 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…This physiological contribution represents a significant fitness benefit in dry habitats like mass grain storage 42 . Here, we demonstrated that the genome of S. silvanidophilus experienced a drastic erosion, resulting in a genome of 308 kbp in size and a strongly AT-biased nucleotide composition (16.2% GC), akin to what has been described for other obligate intracellular 47 , 71 , 72 or extracellular insect symbionts 73 – 76 .…”

Section: Discussionmentioning

confidence: 66%

Inhibition of a nutritional endosymbiont by glyphosate abolishes mutualistic benefit on cuticle synthesis in Oryzaephilus surinamensis

et al. 2021

Self Cite

View full text Add to dashboard Cite

Glyphosate is widely used as a herbicide, but recent studies begin to reveal its detrimental side effects on animals by targeting the shikimate pathway of associated gut microorganisms. However, its impact on nutritional endosymbionts in insects remains poorly understood. Here, we sequenced the tiny, shikimate pathway encoding symbiont genome of the sawtoothed grain beetle Oryzaephilus surinamensis. Decreased titers of the aromatic amino acid tyrosine in symbiont-depleted beetles underscore the symbionts’ ability to synthesize prephenate as the precursor for host tyrosine synthesis and its importance for cuticle sclerotization and melanization. Glyphosate exposure inhibited symbiont establishment during host development and abolished the mutualistic benefit on cuticle synthesis in adults, which could be partially rescued by dietary tyrosine supplementation. Furthermore, phylogenetic analyses indicate that the shikimate pathways of many nutritional endosymbionts likewise contain a glyphosate sensitive 5-enolpyruvylshikimate-3-phosphate synthase. These findings highlight the importance of symbiont-mediated tyrosine supplementation for cuticle biosynthesis in insects, but also paint an alarming scenario regarding the use of glyphosate in light of recent declines in insect populations.

show abstract

Section: Discussionmentioning

confidence: 66%

Inhibition of a nutritional endosymbiont by glyphosate abolishes mutualistic benefit on cuticle synthesis in Oryzaephilus surinamensis

et al. 2021

Self Cite

View full text Add to dashboard Cite

show abstract

“…The critical regulatory decision points thus likely depend less on any decisive nutrient or nutrient-targeting enzyme (e.g. a pectinase) (58), but rather on the decisive cues (e.g. volatile semiochemicals (54, 59)) that enable ants to detect the cultivar’s immediate nutritional needs and then adjust provisioning.…”

Section: Discussionmentioning

confidence: 99%

The multidimensional nutritional niche of fungus-cultivar provisioning in free-ranging colonies of a neotropical leafcutter ant

Crumière

James

Lannes

et al. 2021

Preprint

View full text Add to dashboard Cite

The foraging trails of Atta leafcutter colonies are among the most iconic scenes in Neotropical ecosystems, with thousands of ants carrying freshly cut plant fragments back to their nests where they are used to provision a fungal food crop. We tested a hypothesis that the fungal cultivar's multidimensional requirements for macronutrients (protein and carbohydrates) and minerals (Al, Ca, Cu, Fe, K, Mg, Mn, Na, P and Zn) govern the foraging breadth of Atta colombica leafcutter ants in a Panamanian rainforest. Analyses of freshly cut plant fragments carried by leafcutter foragers showed that the combination of fruits, flowers, and leaves provide for a broad realized nutritional niche that can maximize cultivar's performance. And, while the leaves that comprised the most harvested resource also delivered an intake target containing protein in excess of the amounts that can maximize cultivar growth, in vitro experiments showed that the minerals P, Al, and Fe can enhance the cultivar's tolerance to protein-biased substrates, and potentially expand the ants' foraging niche. Yet, the cultivar also exhibits narrow margins between mineral limitation and toxicity that may render plant fragments with seemingly optimal blends of macronutrients unsuitable for provisioning. Our approach highlights that optimal foraging is inherently multidimensional and links the foraging behavior of a generalist insect herbivore to the fundamental nutritional niche of its microbial symbiont.

show abstract

“…The impacts of symbionts on their individual hosts has both ecological and evolutionary implications. For instance, symbionts can alter the capacity of their host to colonize new ecological niches or change the direction of sexual selection (Dyson and Hurst, 2004; Salem et al , 2020). They may drive host evolution, both to accommodate symbionts with positive effects (for instance, bacteriomes) (Buchner, 1965) and suppress negative symbiont characteristics (Hornett et al 2006).…”

Section: Introductionmentioning

confidence: 99%

Rapid divergence in independent aspects of the compatibility phenotype in the Spiroplasma/Drosophila interaction

Griffin

Gerth

Hurst

2021

Preprint

View full text Add to dashboard Cite

Heritable symbionts represent important components of host biology, both as antagonistic reproductive parasites and as beneficial protective partners. An important component of heritable microbes biology is their ability to establish in new host species, a process equivalent to a host shift for an infectiously transmitted parasite or pathogen. For a host shift to occur, the symbiont must be compatible with the host: it must not cause excess pathology, must have good vertical transmission, and possess a drive phenotype that enables spread. Classically, compatibility has been considered a declining function of genetic distance between novel and ancestral host species. Here we investigate the evolutionary lability of compatibility to heritable microbes by comparing the capacity for a symbiont to establish in two novel host species equally related to the ancestral host. Compatibility of the protective Spiroplasma from D. hydei with D. simulans and D. melanogaster was tested. The Spiroplasma had contrasting compatibility in these two host species. The transinfection showed pathology and low vertical transmission in D. melanogaster but was asymptomatic and transmitted with high efficiency in D. simulans. These results were not affected by the presence/absence of Wolbachia in either of the two species. The pattern of protection was not congruent with that for pathology/transmission, with protection being weaker in the D. simulans, the host in which Spiroplasma was asymptomatic and transmitted well. Further work indicated pathological interactions occurred in D. sechellia and D. yakuba, indicating that D. simulans was unusual in being able to carry the symbiont without damage. The differing compatibility of the symbiont with these closely related host species emphasises first the rapidity with which host-symbiont compatibility evolves despite compatibility itself not being subject to direct selection, and second the independence of the different components of compatibility (pathology, transmission, protection). This requirement to fit three different independently evolving aspects of compatibility, if commonly observed, is likely to be a major feature limiting the rate of host shifts. Moving forward, the variation between sibling species pairs observed above provides an opportunity to identify the mechanisms behind variable compatibility between closely related host species, which will drive hypotheses as to the evolutionary drivers of compatibility variation.

show abstract

Symbiont Digestive Range Reflects Host Plant Breadth in Herbivorous Beetles

Abstract: Highlights d Stammera genomes are structurally conserved across Cassidinae species d Symbiont pectinases complement the host's endogenous cellulases and xylanases d Stammera differentially encode pectinases in their reduced genomes d Symbiont pectinolytic range reflects host plant breadth

Cited by 69 publications

References 90 publications

Inhibition of a nutritional endosymbiont by glyphosate abolishes mutualistic benefit on cuticle synthesis in Oryzaephilus surinamensis

Inhibition of a nutritional endosymbiont by glyphosate abolishes mutualistic benefit on cuticle synthesis in Oryzaephilus surinamensis

The multidimensional nutritional niche of fungus-cultivar provisioning in free-ranging colonies of a neotropical leafcutter ant

Rapid divergence in independent aspects of the compatibility phenotype in the Spiroplasma/Drosophila interaction

Contact Info

Product

Resources

About