Characterization of pioneer microbiomes associated with Apostichopus japonicus: Insights into host-microbe interactions and sustainable aquaculture [an abstract of entire text]

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Characterization of pioneer microbiomes associated with Apostichopus japonicus: Insights into host-microbe
interactions and sustainable aquaculture [an abstract of entire text]

Yu, Juanwen

北海道大学. 博士(水産科学) 甲第15589号

2023-09-25

http://hdl.handle.net/2115/90924

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theses (doctoral - abstract of entire text)

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主論文の要約
博士の専攻分野の名称：博士（水産科学）

氏名：YU JUANWEN

学 位 論 文 題 目
Characterization of pioneer microbiomes associated with Apostichopus japonicus: Insights into hostmicrobe interactions and sustainable aquaculture
（宿主と微生物の相互作用と持続可能な養殖に向けての洞察）
Sea cucumbers (Holothuroidea) are marine organisms known for their commercial value and unique
biological characteristics. They play important roles in marine ecosystems as bioturbators, contributing to sediment
mixing and nutrient cycling. Sea cucumbers possess intriguing biological phenomena such as autolysis, aestivation,
evisceration, and remarkable regenerative capacities, making them excellent model organisms for studying organ
regeneration and understanding the evolutionary context of deuterostomes.
Recent advancements in sequencing technologies and the holobiont and hologenome concepts have
revolutionized our understanding of host-microbiome interactions. The holobiont concept recognizes the host
organism and its associated microbial communities as a collective entity, acknowledging the significant influence
of microbes on host biology. Exploring microbiomes has become crucial in unraveling the role of microorganisms
in various aspects of host biology, including development, growth, health, and disease. The role of pioneer microbes
in the early life microbiome is particularly crucial in shaping later microbiomes and impacting host development
and health. These pioneer microbes contribute to nutrient production, immune system maturation, and the
prevalence of diseases and disorders. Understanding the role of pioneer colonizers provides insights into holobiont
assembly and the long-term effects of early life microbiomes on overall well-being.
With the increasing attention on host-associated microbiomes, the study of microbiomes in sea cucumbers
has gained significance due to their high commercial value and the challenges associated with their sustainable
aquaculture. Investigating the microbial communities associated with sea cucumbers can provide valuable insights
into their growth, health, and disease resistance. Although previous studies have explored the effects of gut
microbiomes on sea cucumber growth and the dynamics of microbiomes during gut regeneration, there is still a
knowledge gap regarding the establishment of microbiomes during larval development, the composition of the core
microbiome, and the occurrence of diseases in sea cucumber holobionts.
Aims of this study is to address these knowledge gaps by assessing the processes of microbial colonization
and the establishment of a healthy core microbiome in sea cucumber holobionts. In Chapter 1, I focused on
establishing a laboratory breeding system to collect fertilized eggs and larvae at different developmental stages of
sea cucumbers. Significant alterations in microbial community structure are observed, particularly in the late
auricularia stage, indicating a correlation between developmental stage and microbiota composition. Additionally,
a total of 257 strains, including potential probiotics, are isolated from sea cucumber larvae across various
developmental stages. These findings shed light on the dynamic changes in the microbiota during early life stages

and suggest that studying the interaction between pioneer colonizers and host sea cucumbers may contribute to the
development of sea cucumber aquaculture.
In Chapter 2, I investigated normal and gut-regenerated fecal samples from sea cucumber adults to isolate
bacterial strains. A total of 153 strains belonging to four genera are identified. A comparison between the
microbiomes of wild and normal specimens reveals potential second pioneer colonizers in gut-regenerated
individuals. Furthermore, a meta16S analysis successfully isolates 115 additional amplicon sequence variants
(ASVs), providing insights into the proportion of cultivable bacteria. These findings contribute to our understanding
of the microbiome reassembly during gut regeneration in sea cucumbers.
In Chapter 3, I focused on metagenomic analyses to assess the core and stage core microbiome during larval
ontogenesis in sea cucumbers. The detection of an early life core microbiome, including pioneer core microbes,
suggests a stepwise establishment of the microbiome related to ontogenesis and feeding behavior. Notably, the
abundance of genome sequences from the growth-promoting bacterium Sulfitobactor strain BL28 is detected in the
metagenomic sequence pool obtained from early-life sea cucumber stages. These findings underscore the critical
role of understanding the core microbiome and associated functions during early life stages in marine invertebrates,
as it offers avenues for enhancing growth, immunity, disease resistance, and holobiont maintenance.
In Chapter 4, the occurrence of intestinal atrophy disease in sea cucumber larvae is reported for the first time.
Metagenomic analysis is employed to elucidate the differences in the microbiome of atrophy larvae. The potential
pathogenic bacterium Tenacibaculum is found as being associated with the development of intestinal atrophy disease.
The study also highlights the significant role of rearing seawater in shaping the microbiome of atrophy larvae and
inducing potential pathogenicity. Further research into the mechanisms and pathogenesis of this disease is necessary
for the sustainable development of the sea cucumber aquaculture industry.
Overall, this study provides a deeper understanding of the complex interactions between sea cucumber hosts
and their microbiomes. The significance of early-life microbiomes in holobiont assembly is highlighted,
emphasizing the importance of microbiome establishment for host development and health. Furthermore, the
identification of core microbiome taxa and their functional implications offers a foundation for monitoring and
managing the health and ecological status of sea cucumber populations. ...

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