Cnidarian-Symbiodiniaceae symbiosis establishment is independent of photosynthesis

Jinkerson, Robert E.; Russo, Joseph; Newkirk, Casandra R.; Kirk, Andrea L; Richard, J.; Martindale, Mark Q.; Grossman, Arthur R.; Hatta, Masayuki; Xiang, T.

doi:10.1016/j.cub.2022.04.021

Cited by 32 publications

(42 citation statements)

References 88 publications

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“…In contrast, hints of endosymbiont control over the host are rare and usually observed in facultative endosymbioses. For instance, recent findings have shown that free-living, facultative symbiotic algae are still able to colonize and proliferate in some species of cnidaria even when impaired in photosynthesis – the main host fitness advantage 41 . This raises the possibility of species-specific events of parasitic-like behavior of algal endosymbionts in contexts of nutrient shortage, similar to what we have observed for S. pierantonius .…”

Section: Discussionmentioning

confidence: 99%

Weevil carbohydrate intake triggers endosymbiont proliferation: a trade-off between host benefit and endosymbiont burden

Dell’Aglio

Lacotte

Peignier

et al. 2022

Preprint

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Nutritional symbiosis between insects and intracellular bacteria (endosymbionts) are a major force of adaptation, allowing animals to colonize nutrient-poor ecological niches. Many beetles feeding on tyrosine-poor substrates rely on a surplus of aromatic amino acids produced by bacterial endosymbionts that synthesize them autotrophically. This surplus of aromatic amino acids is crucial for the biosynthesis of a thick exoskeleton, the cuticle, which is made of a matrix of chitin with proteins and pigments built from the tyrosine-derived 3,4-dihydroxyphenylalanine (DOPA14), providing an important defensive barrier against biotic and abiotic stress. Other endosymbiont-related advantages for beetles include a faster development, and improved fecundity. The association between the cereal weevil Sitophilus oryzae and Sodalis pierantonius endosymbiont19 represents a unique case study: in young adult weevils, endosymbionts undergo a massive proliferation concomitant with the cuticle tanning, then they are fully eliminated. While endosymbiont clearance is a host-controlled process, the mechanism triggering endosymbiont proliferation remains poorly understood. Here, we show that endosymbiont proliferation relies on host carbohydrate intake. Remarkably, insect fecundity was preserved, and the cuticle tanning achieved, even when endosymbiont proliferation was experimentally blocked, except in the context of a severely unbalanced diet. Moreover, a high endosymbiont load coupled with nutrient shortage dramatically impacts host survival, revealing the high energy cost of proliferating endosymbionts and the incapacity of the host to adjust energy allocation.

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Section: Discussionmentioning

confidence: 99%

Weevil carbohydrate intake triggers endosymbiont proliferation: a trade-off between host benefit and endosymbiont burden

Dell’Aglio

Lacotte

Peignier

et al. 2022

Preprint

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“…In the future, genome editing could be better developed to knock out Symbiodiniaceae genes with unknown functions, making it easier to determine their biological roles. UV mutagenesis is a classic method for introducing mutations; it was used recently to create photosynthesis mutants via screening of colored mutants (Jinkerson et al, 2022), but its random nature is less than ideal for reverse genetics. RNA silencing is a more targeted approach that could potentially be exploited in Symbiodiniaceae studies (Zhang and Lin, 2019), but the rapidly advancing CRISPR/Cas9 technology is most desirable for its ability to knock out specific genes.…”

Section: How Can Transcriptomics Proteomics and Single-cell Technique...mentioning

confidence: 99%

Building Consensus around the Assessment and Interpretation of Symbiodiniaceae Diversity

Davies¹,

Gamache²,

Howe‐Kerr³

et al. 2022

Preprint

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Within microeukaryotes, genetic and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellies), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.

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“…To determine whether B. minutum could be used as a delivery agent to the cnidarian host, clonal aposymbiotic specimens of E. diaphana strain H2 were reared in the Jinkerson laboratory and were inoculated with nanocerialoaded B. minutum (control n = 6, treatment n = 6). The inoculation method follows that developed by Jinkerson et al (2022). Anemones used for inoculation were 3-5 mm in length (from the pedal disk to oral disk).…”

Section: Internalization Visualizationmentioning

confidence: 99%

Engineered nanoceria alleviates thermally induced oxidative stress in free-living Breviolum minutum (Symbiodiniaceae, formerly Clade B)

et al. 2022

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The breakdown of symbiotic mutualism between cnidarian hosts and dinoflagellate algae partners (i.e., bleaching) has been linked to an immune-like response pathway brought on by a nitro-oxidative burst, a symptom of thermal stress. Stress induced by reactive oxygen species (ROS)/reactive nitrogen species is a problem common to aerobic systems. In this study, we tested the antioxidant effects of engineered poly(acrylic acid)-coated cerium dioxide nanoparticles (CeO2, nanoceria) on free-living Symbiodiniaceae (Breviolum minutum), a dinoflagellate alga that forms symbiotic relationships with reef-building corals and anemones. Results show that poly(acrylic acid)-coated CeO2 with hydrodynamic diameters of ~4 nm are internalized by B. minutum in under 30 min and subsequently localized in the cytosol. Nanoceria exposure does not inhibit cell growth over time, with the treated cultures showing a similar growth trend over the 25-day exposure. Aerobic activity and thermal stress when held at 34°C for 1 h (+6°C above control) led to increased intracellular ROS concentration with time. A clear ROS scavenging effect of the nanoceria was observed, with a 5-fold decrease in intracellular ROS levels during thermal stress. The nitric oxide (NO) concentration decreased by ~17% with thermal stress, suggesting the rapid involvement of NO scavenging enzymes or proteins within 1 h of stress onset. The presence of nanoceria did not appear to influence NO concentration. Furthermore, aposymbiotic anemones (Exaiptasia diaphana, ex Aiptasia pallida) were successfully infected with nanoceria-loaded B. minutum, demonstrating that inoculation could serve as a delivery method. The ability of nanoceria to be taken up by Symbiodiniaceae and reduce ROS production could be leveraged as a potential mitigation strategy to reduce coral bleaching.

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Cnidarian-Symbiodiniaceae symbiosis establishment is independent of photosynthesis

Cited by 32 publications

References 88 publications

Weevil carbohydrate intake triggers endosymbiont proliferation: a trade-off between host benefit and endosymbiont burden

Weevil carbohydrate intake triggers endosymbiont proliferation: a trade-off between host benefit and endosymbiont burden

Building Consensus around the Assessment and Interpretation of Symbiodiniaceae Diversity

Engineered nanoceria alleviates thermally induced oxidative stress in free-living Breviolum minutum (Symbiodiniaceae, formerly Clade B)

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