Resolving the molecular mechanisms of intracellular coral-algal symbiosis

Project Information

SYMCELLS

Grant agreement ID: 724715

DOI

10.3030/724715

Project closed

EC signature date 17 March 2017

Start date 1 June 2017

End date 31 May 2023

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 2 272 485,00

EU contribution

€ 2 272 485,00

Coordinated by

LUDWIG-MAXIMILIANS-UNIVERSITAET MUENCHEN
Germany

Periodic Reporting for period 5 - SYMCELLS (Resolving the molecular mechanisms of intracellular coral-algal symbiosis)

Reporting period: 2022-06-01 to 2023-05-31

Summary of the context and overall objectives of the project

Symbiotic associations occur in all domains of life and are key drivers of adaption and evolutionary diversification. A prime example is the endosymbiosis between corals and eukaryotic, photosynthetic dinoflagellates which transfer critical nutrients to their coral host. Here, two very distinct cells, an animal host and a dinoflagellate symbiont cell, coordinate their functions to drive the productivity and biodiversity of a whole ecosystem. This highlights the need for understanding the cell biology of endosymbiosis. This is challenging because corals are difficult experimental subjects. Therefore, we apply a unique model systems’ approach using the symbiosis anemone model Aiptasia, modern organismal biology, cell biology, biochemistry, and comparative work with phylogenetically relevant organisms at the bench and corals in the field. Dissecting the cell biology of this endosymbiotic life-style at the mechanistic level is critical to understand its evolution and response to the environment.

Research on coral symbiosis is also timely, since coral reefs are home to >25% of all marine species and provide food and income to millions of people. Thus coral reef ecosystems have major ecological and economic impacts for society. Yet, coral reefs are currently threatened by ‘coral bleaching’ due to climate change. Environmental stress such as the increase in sea water temperature leads to the breakdown of coral-algal symbiosis, which - if not reversed in a timely manner - leads to coral death. Understanding the molecular basis of the symbiotic interaction of corals and their symbionts provides the basis to understand the mechanisms of bleaching and thus the basis to develop effective means to mitigate coral reef loss.

Most corals acquire symbionts anew each generation during larval stages and the first objective of the project aims to uncover the fundamental mechanisms involved in symbiont acquisition and integration into host cells. Nutrient transfer from symbiont to host is vital to the survival of corals in nutrient poor environments and the second objective is to uncover key mechanisms of the metabolic transfer between the partners, as well as exploring the mechanisms of how symbionts can persist intracellularly inside host cells.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

During the project, we investigated distinct aspects of the molecular mechanisms underlying coral symbiosis. We identifies integrins as key molecules for symbiont uptake by the host cell (Jones et al., in prep). We found that immune suppression in the host cell is key for the symbionts to avoid expulsion by 'vomocytosis', and thus stable symbiont intracellurization (Jacobovitz & Rupp et al., Nature Microbiology 2021). We determined that the highly conserved mTOR signalling pathway is co-opted to integrate symbiont derived nutrients into the host cell (Voss et al., Current Biology, 2023). We also identified sterols as key nutrients transferred from symbionts to host. To allow that, the NPC2 gene family has been expanded in symbiotic cnidarians (Hambleton et al., eLife, 2019). Taken together, using our novel model systems' approach to dissect the cell biology of coral-algal endosymbiosis, we made important contributions to a mechanistic understanding of this important symbiotic interaction which is the foundation to coral reef ecosystems. This provides the basis to understand the ecology and evolution of coral symbiosis, a prerequisite to guide reef conservation. Due to our major contributions to the field, we were invited to write a comprehensive review on this topic entitled "Unlocking the Complex Cell Biology of Coral–Dinoflagellate Symbiosis: A Model Systems Approach" (Jacobovitz, Hambleton and Guse; Annual Review of Genetics, in press).


Along the way we also developed various new techniques, protocol and molecular tools to further establish Aiptasia as a model system for the cell biology, ecology and evolution of coral symbiosis. Specifically, we developed a protocol for microinjection to deliver mRNA, protein and DNA to Aiptasia larvae (Jones et al., Scientific Reports 2018), symbiont transformation (Gornik et al, Frontiers in Marine Science, 2022) and larval settlement to close the Aiptasia life cycle (Maegele et al., PNAS, in press). These methods are key to pave the way for a functional analysis of coral symbiosis looking at both partners, cnidarian host and dinoflagellate symbiont.

Finally, we engaged in some side projects during the course of SYMCELLS that are tangential to our analysis of symbiosis and cover the topic of the mechanisms of light sensing in symbiotic cnidarians and its function for adapting to challenging environments (Gornik et al., Molecular Biology and Evolution, 2020 and Kishimoto et al., Scientific Reports, in revision) and a comparative analysis on nutrient allocation in anemones, Garshall et al., bioRxiv doi: 10.1101/2023.05.15.540851).

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

We made significant progress beyond the state-of-the art. We concluded a first set of newly developed tools and resources for Aiptasia larvae, a major milestone in establishing a novel model system to dissect the mechanisms of coral-algal endosymbiosis. Taking advantages of our toolbox including molecular techniques, high-resolution microscopy, biochemistry and comparative analyses in field-collected corals, we significantly advanced our understanding of the molecular mechanism underlying coral-algal symbiosis. More broadly, we generated a first molecular framework of the individual steps involved in symbiosis establishment. The steps include symbiont recognition, uptake via phagocytosis, integration into host cell function, interaction with host defence mechanisms and the metabolic transfer between the partners. This mechanistic analysis of these steps has broader implications within the fields of ecology and evolution, and specifically important ramifications on coral reef ecosystem health.

Aiptasia anemone

symbiotic Aiptasia larva