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.

Distinct microbiota assembly mechanisms revealed in different reconstruction stages during gut regeneration in the sea cucumber Apostichopus japonicus

“…Moreover, the microbial community composition in the sea cucumber gut at 42-56 dpe was notably different from that at the initial stage, suggesting the formation of a novel microbiota during gut regeneration. Moreover, this result is consistent with previous findings in the sea cucumber Sclerodactyla briareus and A. japonicus (Weigel, 2020;Yamazaki et al, 2020). Similarly, the source tracking results suggest that the A. japonicus gut bacterial community is reconstructed from the bacterial community present in the residual esophagus and stomach after evisceration.…”

“…Moreover, this result is consistent with previous findings in the sea cucumber Sclerodactyla briareus and A . japonicus (Weigel, 2020 ; Yamazaki et al, 2020 ). Similarly, the source tracking results suggest that the A .…”

“…Gut microbiota succession occurs due to host‐microbe and microbe‐microbe interactions, which are strongly influenced by host physiology and environmental factors (Stephens et al, 2016 ). Several studies have focused on the gut microbiota assembly that occurs during gut regeneration in sea cucumbers (Weigel, 2020 ; Yamazaki et al, 2020 ; Zhang et al, 2020 ). However, the samples collected in these studies were mainly of newly regenerated gut or feces after the lumen has formed, and little is known about the microbiota in the initial stage of regeneration.…”

Genome-wide DNA methylation and transcription analysis reveal the potential epigenetic mechanism of heat stress response in the sea cucumber Apostichopus japonicus

“…Tnr plays an important role in the development of the nervous system, the regeneration of tissues and organs after trauma and it can regulate the morphology of extracellular matrix (Meloty-Kapella et al, 2006). Another study showed that tnr could act as an important ECM component involved in neurodevelopmental regeneration and participates in the intestinal regeneration of A. japonicus (Yamazaki et al, 2020). We speculated that A. japonicus could repair tissue damage during heat stress and resist environmental changes by up-regulating the expression of tnr.…”

Characterization of Microbiomes Associated With the Early Life Stages of Sea Cucumber Apostichopus japonicus Selenka

“…After the recent findings of potential physiological roles in gut microbiomes of the sea cucumber A. japonicus (Yamazaki et al, 2016), dynamics of the microbiome, in particular How sea cucumbers shape their microbiomes? has been a central question (Yamazaki et al, 2020). Among a series of studies on the sea cucumber microbiome, first colonizers on the animal guts called Pioneer Microbes are worth studying in sea cucumbers as they potentially contribute to improving aquaculture technology and accumulate biological knowledge on gut microbiome evolution compared to those in humans (Wopereis et al, 2014).…”