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Unravelling the Metabolic Interactions of the Aiptasia-Symbiodiniaceae Symbiosis

Many omics-level studies have been undertaken on Aiptasia, however, our understanding
of the genes and processes associated with symbiosis regulation and maintenance is still
limited. To gain deeper insights into the molecular processes underlying this association, we investigated this relationship using multipronged approaches combining next
generation sequencing with metabolomics and immunohistochemistry.
We identified 731 high-confident symbiosis-associated genes using meta-analysis.
Coupled with metabolomic profiling, we exposed that symbiont-derived carbon enables
host recycling of ammonium into nonessential amino acids, which may serve as a
regulatory mechanism to control symbiont growth through a carbon-dependent negative
feedback of nitrogen availability to the symbiont.
We then characterized two symbiosis-associated ammonium transporters (AMTs). Both of
the proteins exhibit gastrodermis-specific localization in symbiotic anemones. Their tissuespecific
localization consistent with the higher ammonium assimilation rate in
gastrodermis of symbiotic Aiptasia as shown by 15N labeling and nanoscale secondary ion
mass spectrometry (NanoSIMS). Inspired by the tissue-specific localization of AMTs, we
investigated spatial expression of genes in Aiptasia. Our results suggested that symbiosis
with Symbiodiniaceae is the main driver for transcriptional changes in Aiptasia. We
focused on the phagosome-associated genes and identified several key factors involved in
phagocytosis and the formation of symbiosome. Our study provided the first insights into
the tissue specific complexity of gene expression in Aiptasia.
To investigate symbiosis-induced response in symbiont and to find further evidence for the
hypotheses generated from our host-focused analyses, we explored the growth and gene
expression changes of Symbiodiniaceae in response to the limitations of three essential
nutrients: nitrogen, phosphate, and iron, respectively. Comparisons of the expression
patterns of in hospite Symbiodiniaceae to these nutrient limiting conditions showed a
strong and significant correlation of gene expression profiles to the nitrogen-limited culture condition. This confirmed the nitrogen-limited growing condition of Symbiodiniaceae in
hospite, and further supported our hypothesis that the host limits the availability of nitrogen,
possibly to regulate symbiont cell density.
In summary, we investigated different molecular aspects of symbiosis from both the host’s
and symbiont’s perspective. This dissertation provides novel insights into the function of
nitrogen, and the potential underlying molecular mechanisms, in the metabolic interactions
between Aiptasia and Symbiodiniaceae.

Identiferoai:union.ndltd.org:kaust.edu.sa/oai:repository.kaust.edu.sa:10754/630118
Date12 1900
CreatorsCui, Guoxin
ContributorsAranda, Manuel, Biological and Environmental Sciences and Engineering (BESE) Division, Gojobori, Takashi, Voolstra, Christian R., Pringle, John R., Weis, Virginia M.
Source SetsKing Abdullah University of Science and Technology
LanguageEnglish
Detected LanguageEnglish
TypeDissertation
Rights2019-12-03, At the time of archiving, the student author of this dissertation opted to temporarily restrict access to it. The full text of this dissertation became available to the public after the expiration of the embargo on 2019-12-03.

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