The Structure and Function of Gut Microbiomes of Two Species of Sea Urchins, Mesocentrotus nudus and Strongylocentrotus intermedius, in Japan

Abstract

Sea urchin is an indicator of coastal environmental changes in the global warming era, and is also a model organism in developmental biology and evolution. Due to the depletion of wild resources, new aquaculture techniques for improving stocks have been well studied. The gut microbiome shapes various aspects of a host’s physiology. However, these microbiome structures and functions on sea urchins, particularly Mesocentrotus nudus and Strongylocentrotus intermedius which are important marine bioresources commonly found in Japan, have not been fully investigated yet. Using metagenomic approaches including meta16S and shotgun metagenome sequencings, the structures, functions, and dynamics of the gut microbiome of M. nudus and S. intermedius, related to both habitat environment and host growth, were studied. Firstly, a broad meta16S analysis revealed that at the family level, Psychromonadaceae and Flavobacteriaceae reads (38–71%) dominated in these sea urchins, which is a unique feature observed in species in Japan. Flavobacteriaceae reads were more abundant in individuals after rearing in an aquarium with circulating compared to one with running water. Campylobacteraceae and Vibrionaceae abundances increased in both kinds of laboratory-reared sea urchins in both types of experiments. 2-weeks feeding experiments of M. nudus and S. intermedius transplanted from the farm to laboratory revealed that these gut microbial structures were affected by diet rather than rearing environments and host species. Secondly, further meta16S analysis of microbial reads related to M. nudus growth revealed that at least four Amplicon Sequence Variant (ASV) affiliated to Saccharicrinis fermentans, which is known to be a nitrogen (N2) fixing bacterium, showed a significant positive correlation to the body weight and test diameter. Interestingly, gut microbiome comparisons using shotgun metagenome sequencing of individuals showing higher and lower growth rates revealed a significant abundance of “Nitrate and nitrite ammonification” genes in the higher-grown individuals under the circulating water rearing. These findings provide new insights on the structure-function relationship of sea urchin gut microbiomes beyond previously reported nitrogen fixation function in sea urchin in 1950s; we discovered a nitrate reduction function into ammonium for the growth promotion of sea urchin.

Alterations in sea urchin (Mesocentrotus nudus) microbiota and their potential contributions to host according to barren severity

“…Seawater temperature and host growth status could influence the microbiota in sea urchins as well as the dispersal of surrounding microbiota. Although the growth stage was associated with the gut microbiome of M. nudus in a previous study 35 , host growth status was associated only with the pharynx microbiota in the present study, and environmental factors were more significant factors in the variation of the microbiota. This difference could be owing to the different experimental designs of the studies.…”

“…Environmental conditions and host factors influence the microbiota in sea urchins as well as the microbiota in the surrounding environments. A previous study reported an association between the microbiota and sea urchin growth stage (body weight and shell length) 35 . Therefore, we analyzed whether environmental or host growth factors are strongly associated with the microbiota in the pharynx or gut using the EnvFit model (Supplementary Table 3 ).…”

“…These results indicate that the gut microbiota of sea urchins in severely barren regions could play different roles in host energy metabolism with limited feeding algae. Although the effect of diet on the gut microbiota of sea urchins has been reported 35 , 44 , the influence of urchin barren on the microbiota of sea urchins is limited. Therefore, our results can provide insights into the interactions between gut microbiota and sea urchins under limited dietary conditions of urchin barren in natural habitats.…”

Effects of sea urchin feces on behaviors, digestion ability, growth, and resistance of the sea cucumber Apostichopus japonicus

“…The present study clearly indicates that fecal diet significantly influences the intestinal bacteria of sea cucumbers. Similar phenomenon has been documented in a variety of species, indicating that intestinal bacteria shaping mechanisms are evolutionarily conserved (Wilson et al, 2020;Haditomo et al, 2021).…”

Modest Dietary Protein Requirement for Sea Urchin Gonad Production Demonstrated by Feeding Trials with Consideration of Protein Leaching

“…Although the contribution of cellulolytic bacteria to cellulose digestion has been predicted in the wood-feeding sea urchin Asterechinus elegans [93], Watts et al [94] considered that insoluble fiber (cellulose) is essentially not digested in sea urchins. Moreover, abundance of cellulase genes was rare (<0.1%) in the metagenome sequences of the M. nudus gut microbe [95]. Thus, we used cellulose as a filler to balance diets with different protein contents to eliminate the effects of dietary contents other than protein.…”