Responses of Gut Microbial Community Composition and Function of the Freshwater Gastropod Bellamya aeruginosa to Cyanobacterial Bloom

Abstract

Freshwater gastropods are widely distributed and play an important role in aquatic ecosystems. Symbiotic microorganisms represented by gut microbes can affect the physiological and biochemical activities of their hosts. However, few studies have investigated the response of the gut microbial community of snails to environmental stress. In this study, the dynamics of the gut microbiota of the gastropod Bellamya aeruginosa were tracked to explore their responses in terms of their composition and function to cyanobacterial bloom. Differences in gut microbial community structures during periods of non-cyanobacterial bloom and cyanobacterial bloom were determined. Results showed that the alpha diversity of the gut microbiota exposed to cyanobacterial bloom was lower than that of the gut microbiota exposed to non-cyanobacterial bloom. The main genera differentiating the two periods were Faecalibacterium, Subdoligranulum, Ralstonia, and Pelomonas. Microcystins (MCs) and water temperature (WT) were the primary factors influencing the gut microbial community of B. aeruginosa; between them, the influence of MCs was greater than that of WT. Fourteen pathways (level 2) were notably different between the two periods. The pathways of carbohydrate metabolism, immune system, environmental adaptation, and xenobiotics biodegradation and metabolism in these differential pathways exhibited a strong linear regression relationship with MCs and WT. Changes in the functions of the gut microbiota may help B. aeruginosa meet its immunity and energy needs during cyanobacterial bloom stress. These results provide key information for understanding the response pattern of freshwater snail intestinal flora to cyanobacterial blooms and reveal the underlying environmental adaptation mechanism of gastropods from the perspective of intestinal flora.

Integration of Transcriptomics and Microbiomics Reveals the Responses of Bellamya aeruginosa to Toxic Cyanobacteria

“…These results are similar to those reported by Duan et al [ 53 ]. However, this finding is contrary to the results of the previous field investigation [ 30 ], which may be related to the complex and variable environmental conditions in the field. Toxic cyanobacterial exposure also altered the community composition of gut microorganisms, increasing the relative abundance of Firmicutes ( Table S3 ).…”

“…Toxic cyanobacterial exposure also altered the community composition of gut microorganisms, increasing the relative abundance of Firmicutes ( Table S3 ). In general, Proteobacteria, Bacteroidota, and Firmicutes were the three most abundant phyla in the intestinal microbiota of freshwater snails [ 30 ], generally consistent with the results in this paper. Members of the phylum Firmicutes are thought to regulate host energy metabolism by producing short-chain fatty acids [ 54 ].…”

“…Therefore, the MCs concentration in this analysis was regarded as the equivalents of MC-LR. In addition, the matrix effect and the recovery of MC extraction were determined, and they were consistent with previous results [ 30 ]. The average extraction efficiency was 91.6%, and the matrix effect was almost negligible due to small differences between methanol and the matrix results, with an average of 4.3%.…”

“…Members of the phylum Firmicutes are thought to regulate host energy metabolism by producing short-chain fatty acids [ 54 ]. In the T group, the abundance of some genera with the ability to degrade MCs increased, such as Pseudomonas , Lactobacillus , and Ralstonia ( Table S4 ), in line with the results of the field experiment that showed the abundance of Ralstonia and Pseudomonadales increased after cyanobacterial bloom outbreak [ 30 ]. These results may suggest that toxic cyanobacterial stress makes the MCs-degrading flora more competitive and other microbiota less competitive.…”

“…The bioaccumulation and distribution of MCs in gastropods, whether exposed in the field [ 30 ] or experimentally [ 31 ], have been widely reported, and the highest accumulated organ is the hepatopancreas [ 32 ]. In our case, Bellamya accumulated a large amount of MCs at the beginning of the exposure test and decreased at a later stage, similar to the results of previous studies [ 10 , 33 ].…”