Changes in Symbiotic Microbiota and Immune Responses in Early Development Stages of Rapana venosa (Valenciennes, 1846) Provide Insights Into Immune System Development in Gastropods

Abstract

The symbiotic microbiota can stimulate modulation of immune system, which also can promote immune system mature in critical developmental periods. In this study, we have investigated the symbiotic microbiota in Rapana venosa at five early development stages using Illumina high-throughput sequencing, and detected immune responses in larvae. Analysis of the symbiotic microbiota sequences identified that the most abundant phylum was Proteobacteria. Beta diversity analysis indicated that the structure of the symbiotic microbiota dramatically shifted in early development stages. The abundance of immune-related KEGG Orthologs (KOs) also increased in competent larval (J4, 30-day post-hatching) and postlarval after 3 days of metamorphosis (Y5, 33-day post-hatching) stages. Acid phosphatase activity decreased significantly in the Y5 stage, and alkaline phosphatase activity also at a lower level in Y5 stage, whereas lysozyme activities exhibited no remarkable change. Also, the activities of catalase and superoxide dismutase activities decreased dramatically during early development stages of R. venosa. Dramatic changes in the symbiotic microbiota and the immune response mainly occurred in the initially hatched veliger (C1), competent larval (J4) and postlarval (Y5) stages, during which the hosts might experience substantial environmental changes or changes in physiological structure and function. These findings expand our understanding of the stage-specific symbiotic microbiota in R. venosa and the close association between immune system and symbiotic microbiota in mollusks, however, the specific relationship may need more researches are needed to investigated in the future.

Symbiotic microbiome and metabolism profiles reveal the effects of induction by oysters on the metamorphosis of the carnivorous gastropod Rapana venosa

“…2 B (low-abundance OTUs (<0.05) were merged into “others”); 7 of them belonged to Alphaproteobacteria, Gammaproteobacteria, and Proteobacteria, and 2 belonged to Cyanobacteria. Proteobacteria and Cyanobacteria were the most abundant phyla in the symbiotic microbiota in R. venosa , consistent with our previous studies [31] . At the genus level, norank_f__norank_o__Chloroplast was the most dominant genus in the Ce and Cl groups (control), and its relative abundance was more than 45%; norank_f__norank_o__Chloroplast was still the most dominant genus in the Oe group, but its relative abundance decreased to 37.47%.…”

“…In this study, induction by juvenile oyster increased the expression of carboxypeptidase while slightly decreasing the expression of cellulase ( Fig. 1 ), which is consistent with the change in food habit transition during the metamorphosis of R. venosa [20] , [31] , [35] . Our results suggest that the digestive system of the R. venosa larvae responded to the induction by juvenile oysters and that digestive enzyme expression changed to meet the needs of food habit transition and metamorphosis, which is consistent with a previous study in grass carp showing that feeding plants to juvenile grass carp in advance can promote the development of its digestive system and change the activity of digestive enzymes [25] .…”

“…The Ce and Oe groups were relatively close ( Fig. 3 E), which suggested that both the short development period (10 h) and the induction by oysters had significant effects on the structure of the symbiotic microflora of the larvae, and the former had been reported in our previous study [31] .

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“…Meanwhile, growing evidence supports that the symbiotic microbiota plays a key role in regulating host digestive and metabolic functions [28] . Cavalcanti et al [30] reviewed the vital impact of bacteria on the metamorphosis of invertebrates, and we also found dramatic alterations in symbiotic microbiota during metamorphosis in R. venosa [31] . Therefore, we hypothesize that symbiotic microbiota may play an important role in regulating the alteration of the digestive system and neuroendocrine system in the metamorphosis mentioned above.…”

“…Previous studies have shown that symbiotic microbiota and metabolic profiles are dramatically altered with larval development during metamorphosis [21] , [31] . Here, we attempted to determine the main induction effect of juvenile oysters on R. venosa and reveal the regulatory mechanism of metamorphosis induced by juvenile oysters from the perspective of the digestive system and neuroendocrine system.…”