Deciphering the Cellular Mechanisms Underlying Deep-Sea Chemosynthetic Symbiosis in the Mussel Gigantidas platifrons Using Single-Nucleus RNA-Sequencing

Concetti Chiave

The deep-sea mussel Gigantidas platifrons maintains a stable and efficient chemosynthetic symbiosis with endosymbiotic bacteria through specialized cell types and their coordinated functions in the gill.

Sintesi

The study constructed a comprehensive cell atlas of the gill in the deep-sea mussel Gigantidas platifrons using single-nucleus RNA-sequencing (snRNA-seq) and whole-mount in situ hybridization.

Key insights:

• 13 distinct cell types were identified, including three previously unknown ones, revealing the intricate tissue heterogeneity in the gill.
• The supportive cells, ciliary cells, proliferation cells, and bacteriocytes (symbiont-hosting cells) work together to maintain the gill's structure and function, create an optimal environment for chemosynthesis, and effectively acquire nutrients from the endosymbiotic bacteria.
• Analysis of snRNA-seq data from in situ transplanted mussels showed cell-type specific responses to environmental changes, with bacteriocytes exhibiting the most significant transcriptional changes under methane starvation.
• Bacteriocytes employ specialized mechanisms, such as lysosomal digestion and nutrient transport, to interact with and obtain nutrients from the endosymbionts.
• The study provides insights into the principles of host-symbiont interaction and the bivalves' environmental adaptation mechanisms.

Statistiche

"The gill of G. platifrons contains a high amount of bacterial lipids, which are directly utilised by the host to synthesise most of its lipid contents."
"Genes encoding ribosomal proteins are highly expressed in the bacteriocytes under the methane-rich 'Fanmao' state, suggesting an active protein synthesis and cellular metabolism."
"Under a methane-limited environment, the starved mussels more actively consumed endosymbionts through the 'farming' pathway."
"After being moved back to the methane-rich environment, mussels produced more glutamates which sustained the regrowth of symbionts."

Citazioni

"The ecological success of the bathymodioline symbioses is apparent: the bathymodiolin mussels are often among the most dominant species in the deep-sea chemosynthetic ecosystems."
"Solute carriers may play crucial roles in shuttling nutrients in and out of bacteriocytes and in maintaining the suitable intracellular micro-environment for the symbiont."
"The beating ciliary cells controlled the water flow, providing bacteriocytes with necessary inorganic substances from the environment."

Approfondimenti chiave tratti da

Deciphering deep-sea chemosynthetic symbiosis by single-nucleus RNA-sequencing

by Wang,H., He,... alle www.biorxiv.org 05-31-2023

https://www.biorxiv.org/content/10.1101/2023.05.29.542712v2

Domande più approfondite

How do the different cell types in the gill coordinate their functions to maintain the stability and efficiency of the host-symbiont relationship over the mussel's lifespan?

In the deep-sea chemosynthetic mussels, such as Gigantidas platifrons, the various cell types in the gill work together in a coordinated manner to support the host-symbiont relationship. The supportive cells, including inter lamina cells, basal membrane cells (BMC)1, BMC2, and mucus cells, play crucial roles in maintaining the anatomical structure of the gill and providing a suitable environment for symbiosis. Inter lamina cells help connect the two layers of basal membranes, while BMC1 and BMC2 contribute to building and stabilizing the basal lamina. Mucus cells, on the other hand, are involved in immune responses and potentially in capturing food particles for the mussel.
The ciliary cells, such as apical ridge ciliary cells, food groove ciliary cells, lateral ciliary cells, and intercalary cells, are responsible for creating water flow to provide necessary substances for the symbionts. Smooth muscle cells, identified in this study, likely assist in gill contraction and ciliary movement. Proliferation cells, including the budding zone cells, dorsal end proliferation cells, and ventral end proliferation cells, continuously generate new cells, including bacteriocytes, which host the symbionts.
Bacteriocytes, the specialized cells hosting the endosymbionts, play a central role in the host-symbiont relationship. They have structural adaptations for harboring, transporting, and digesting the symbionts. The bacteriocytes obtain nutrients from the endosymbionts through lysosomal digestion and potentially through the "milking" pathway, where symbiont-produced nutrients are directly utilized by the host mussel. The coordination among these different cell types ensures the stability and efficiency of the host-symbiont relationship over the mussel's lifespan.

How do the different cell types in the gill coordinate their functions to maintain the stability and efficiency of the host-symbiont relationship over the mussel's lifespan?

The specialized cell types and their interactions observed in deep-sea chemosynthetic mussels, like Gigantidas platifrons, compared to their shallow-water counterparts, are likely driven by specific evolutionary adaptations to the deep-sea environment and the unique symbiotic relationships these mussels have with their endosymbionts.
In the deep-sea environment, where resources are limited and extreme conditions prevail, the gill structure of deep-sea mussels has undergone remarkable adaptations to support their chemosynthetic lifestyle. The presence of unique cell types, such as inter lamina cells, BMC1, BMC2, mucus cells, ciliary cells, and proliferation cells, reflects the need for specialized functions to maintain the stability and efficiency of the host-symbiont relationship. These adaptations may have evolved over time to optimize nutrient acquisition, structural support, and immune responses in the deep-sea environment.
The interactions among these specialized cell types are likely shaped by the selective pressures of the deep-sea ecosystem, where efficient utilization of symbiont-produced nutrients and adaptation to environmental fluctuations are essential for survival. The presence of specific genes and pathways in these cell types, as revealed by single-nucleus RNA sequencing, highlights the molecular mechanisms underlying these evolutionary adaptations.

Could the insights gained from the deep-sea mussel symbiosis be applied to understand host-microbiome interactions in other complex ecosystems, such as the human gut?

The insights gained from studying the deep-sea mussel symbiosis, particularly the coordination of different cell types in maintaining the host-symbiont relationship, can indeed provide valuable lessons for understanding host-microbiome interactions in other complex ecosystems, including the human gut.
The deep-sea mussel symbiosis represents a highly specialized and efficient system where the host and symbiont work together to thrive in extreme environments. By dissecting the cellular and molecular mechanisms of this symbiosis, researchers can uncover general principles of host-microbiome interactions, such as nutrient exchange, immune modulation, and structural support.
The coordination among different cell types in the deep-sea mussel gill mirrors the complex interactions between host cells and the microbiome in the human gut. Understanding how these cell types communicate and collaborate to maintain symbiosis can provide insights into how the human gut microbiome influences host health and metabolism.
By applying the knowledge gained from deep-sea mussel symbiosis to the study of the human gut microbiome, researchers can potentially uncover novel therapeutic targets, diagnostic markers, and treatment strategies for various gut-related disorders and diseases. The parallels between these two ecosystems highlight the universality of host-microbiome interactions and the potential for cross-disciplinary insights.