THESIS
2020
xvi, 253 pages : illustrations (some color) ; 30 cm
Abstract
The rich diversity of chemosymbiotic animals are most common in deep-sea chemosynthesis-based
ecosystems, and represent a pinnacle of harmonic coexistence between microbes and
metazoans. However, the molecular mechanisms of such symbiosis are still largely unclear.
Especially, some host animals still possess a functional gut that can be considered as a critical
mixotrophic dependency in such holobionts. Uncovering the complex interactions among the
symbiotic parties is key to understanding how they cooperate as a single metabolically balanced
unit – holobiont. Here, simultaneous and comprehensive analyses of the hologenome,
holotranscriptome, and holoproteome of deep-sea chemosymbiotic invertebrates were
conducted, to unravel host-microbiota interactions. This collection contri...[
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The rich diversity of chemosymbiotic animals are most common in deep-sea chemosynthesis-based
ecosystems, and represent a pinnacle of harmonic coexistence between microbes and
metazoans. However, the molecular mechanisms of such symbiosis are still largely unclear.
Especially, some host animals still possess a functional gut that can be considered as a critical
mixotrophic dependency in such holobionts. Uncovering the complex interactions among the
symbiotic parties is key to understanding how they cooperate as a single metabolically balanced
unit – holobiont. Here, simultaneous and comprehensive analyses of the hologenome,
holotranscriptome, and holoproteome of deep-sea chemosymbiotic invertebrates were
conducted, to unravel host-microbiota interactions. This collection contribute to understanding
the evolution, ecological and health effects of microorganisms on the host and developing a
suitable toolbox to better characterize deep-sea chemosymbiosis. In a typical endosymbiosis
model, the interdependence between Paraescarpia echinospica and its symbionts was revealed
by mutual nutrient provisions, regulation, and constraints, which is a key adaptation allowing
the tubeworm to thrive in cold-seep chemosynthetic ecosystems. Genomic comparisons of
vestimentiferan endosymbionts showed that the seep-living siboglinid endosymbionts are more
prone than the vent-dwelling siboglinid endosymbionts to resist environmental stress and use
pathogen-like mechanisms to evade host immune responses to survive intracellularly.
Furthermore, the endosymbiont of Paraescarpia echinospica may be able to degrade host
proteins, and the endosymbiont is believed to have evolved strategies to mediate host innate
immunity. Overall, the results shed light on the host-symbiont interactions in maintaining
symbiosis in deep-sea tubeworms and underline the differences between and within symbionts
of vent and seep tubeworm species on the whole genome level. In a semi-endosymbiosis model, the previously overlooked gut ectosymbiosis was supposed to be an essential part of the
holobiont in such animals via using Alviniconcha marisindica as a model in this study.
Individual components of a tripartite system in the Alviniconcha marisindica holobiont lack the
full suite of biochemical pathways necessary to thrive on its own. Endogeneic energy
conversion in the gill (with endosymbionts) and exogenic resource sequestration in the gut (with
ectosymbionts) expanded the energy utilisation in the holobiont system. Interplay among the
symbiotic parties within a holobiont and the influence of external environment are clarified.
The two types of symbiont systems are equipped with different host-specific evasion techniques,
and the host also adopts different corresponding approaches to form and maintain a stable
Alviniconcha marisindica holobiont. Distinct strategies of symbiosis maintenance contribute to
the complexity of the persistent symbioses. Taken together, the work in this thesis revises and
broadens the concept of chemosymbiosis and highlights internal and external interplays among
host, symbionts and deep-sea chemosynthetic ecosystems. This work indicates that
chemosymbioses, and symbiosis as a whole, are even more complex than previously realized.
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