Dataset Information

Tracking the dynamics of individual gut microbiome of sea cucumber Apostichopus japonicus during gut regeneration.

ABSTRACT: Sea cucumbers possess the remarkable capacity to regenerate their body parts or organs. Regeneration of host organs and/or body parts involves reconstruction of the host associated microbiota, however, the dynamics and contribution of microbiota to the regeneration process are largely unknown due to a lack of experimental models. To track the dynamics of individual gut microbiomes during gut regeneration, both caged mariculture and laboratory isolator systems of sea cucumbers (Apostichopus japonicus) were developed and longitudinal meta16S analyses were performed. Under natural environmental conditions in the caged mariculture system, both bacterial and eukaryotic communities in sea cucumbers' guts appeared to be reconstructed within 4 months after evisceration. Using the laboratory isolator, which can trace daily dynamics, we found that fecal microbiota collected before evisceration were clearly different from those collected after evisceration. We also identified eight key bacteria, belonging to Alteromonadaceae, Rhodobacteraceae, Oceanospirillaceae and family-unassigned Gammaproteobacteria, suggesting that these bacteria might interact with the host during the gut regeneration process. Six of the eight key bacteria were isolated for further bioassay using the isolator developed in this study to test whether these isolates affect gut regeneration.

SUBMITTER: Yamazaki Y

PROVIDER: S-EPMC7718794 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Tracking the dynamics of individual gut microbiome of sea cucumber <i>Apostichopus japonicus</i> during gut regeneration.

Yamazaki Yohei Y Sakai Yuichi Y Yu Juanwen J Mino Sayaka S Sawabe Tomoo T

PeerJ 20201201

Sea cucumbers possess the remarkable capacity to regenerate their body parts or organs. Regeneration of host organs and/or body parts involves reconstruction of the host associated microbiota, however, the dynamics and contribution of microbiota to the regeneration process are largely unknown due to a lack of experimental models. To track the dynamics of individual gut microbiomes during gut regeneration, both caged mariculture and laboratory isolator systems of sea cucumbers (<i>Apostichopus ja ...[more]

PMID: 33344070

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Project description:BACKGROUND: Sea cucumbers are a special group of marine invertebrates. They occupy a taxonomic position that is believed to be important for understanding the origin and evolution of deuterostomes. Some of them such as Apostichopus japonicus represent commercially important aquaculture species in Asian countries. Many efforts have been devoted to increasing the number of expressed sequence tags (ESTs) for A. japonicus, but a comprehensive characterization of its transcriptome remains lacking. Here, we performed the large-scale transcriptome profiling and characterization by pyrosequencing diverse cDNA libraries from A. japonicus. RESULTS: In total, 1,061,078 reads were obtained by 454 sequencing of eight cDNA libraries representing different developmental stages and adult tissues in A. japonicus. These reads were assembled into 29,666 isotigs, which were further clustered into 21,071 isogroups. Nearly 40% of the isogroups showed significant matches to known proteins based on sequence similarity. Gene ontology (GO) and KEGG pathway analyses recovered diverse biological functions and processes. Candidate genes that were potentially involved in aestivation were identified. Transcriptome comparison with the sea urchin Strongylocentrotus purpuratus revealed similar patterns of GO term representation. In addition, 4,882 putative orthologous genes were identified, of which 202 were not present in the non-echinoderm organisms. More than 700 simple sequence repeats (SSRs) and 54,000 single nucleotide polymorphisms (SNPs) were detected in the A. japonicus transcriptome. CONCLUSION: Pyrosequencing was proven to be efficient in rapidly identifying a large set of genes for the sea cucumber A. japonicus. Through the large-scale transcriptome sequencing as well as public EST data integration, we performed a comprehensive characterization of the A. japonicus transcriptome and identified candidate aestivation-related genes. A large number of potential genetic markers were also identified from the A. japonicus transcriptome. This transcriptome resource would lay an important foundation for future genetic or genomic studies on this species.

Project description:The gut microbiome has far-reaching effects on host organism health, so understanding the processes that underlie microbial community assembly in the developing gut is a current research priority. Here, a holothurian (also known as sea cucumber; phylum Echinodermata) host is explored as a promising model system for studying the assembly of the gut microbiome. Holothurians have a unique capacity for evisceration (expulsion of the internal organs), followed by rapid regeneration of the gut, decoupling host ontogeny from gut tissue development and permitting experimental manipulation of the gut microbiome in mature host individuals. Here, evisceration was induced in the sea cucumber Sclerodactyla briareus, and regenerating stomach and intestine microbiomes were characterized before and on days 0, 13, 17, and 20 after evisceration using Illumina sequencing of 16S rRNA genes. Regenerating stomach and intestine tissues had microbial communities significantly different from those of mature tissues, with much higher alpha diversity and evenness of taxa in regenerating tissues. Despite immersion in a diverse pool of sediment and seawater microbes in flowthrough seawater aquaria, regenerating gut microbiomes differed at each stage of regeneration and displayed a highly similar community structure among replicates, providing evidence for deterministic host selection of a specific microbial consortium. Moreover, regenerating gut tissues acquired a microbiome that likely conferred energetic and immune advantages to the sea cucumber host, including microbes that can fix carbon and degrade invading pathogens.IMPORTANCE The gut microbiome is pertinent to many aspects of animal health, and there is a great need for natural but tractable experimental systems to examine the processes shaping gut microbiome assembly. Here, the holothurian (sea cucumber) Sclerodactyla briareus was explored as an experimental system to study microbial colonization in the gut, as S. briareus individuals have the ability to completely eviscerate and rapidly regenerate their digestive organs. After induced evisceration, microbial community assembly was characterized over 20 days in regenerating animals. This study demonstrated that colonization of the sea cucumber gut was deterministic; despite immersion in a diverse consortium of environmental microbes, a specific subset of microbes proliferated in the gut, including taxa that likely conferred energetic and immune advantages to the host. Sea cucumbers have the potential to revolutionize our understanding of gut microbiome assembly, as rapid and repeatable gut tissue regeneration provides a promising and tractable experimental system.

Dataset Information

Tracking the dynamics of individual gut microbiome of sea cucumber Apostichopus japonicus during gut regeneration.

Publications

Tracking the dynamics of individual gut microbiome of sea cucumber <i>Apostichopus japonicus</i> during gut regeneration.

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