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. 2023 Mar 14:14:1090899.
doi: 10.3389/fmicb.2023.1090899. eCollection 2023.

Trophic diversification and parasitic invasion as ecological niche modulators for gut microbiota of whitefish

Elena N Kashinskaya  1   2 , Evgeniy P Simonov  1   2 , Larisa G Poddubnaya  3 , Pavel G Vlasenko  1   2 , Anastasiya V Shokurova  1   2 , Aleksey N Parshukov  4 , Karl B Andree  5 , Mikhail M Solovyev  1   2   6
Affiliations

Trophic diversification and parasitic invasion as ecological niche modulators for gut microbiota of whitefish

Elena N Kashinskaya et al. Front Microbiol. .

Erratum in

Abstract

Introduction: The impact of parasites on gut microbiota of the host is well documented, but the role of the relationship between the parasite and the host in the formation of the microbiota is poorly understood. This study has focused on the influence that trophic behavior and resulting parasitism has on the structure of the microbiome.

Methods: Using 16S amplicon sequencing and newly developed methodological approaches, we characterize the gut microbiota of the sympatric pair of whitefish Coregonus lavaretus complex and the associated microbiota of cestodes parasitizing their intestine. The essence of the proposed approaches is, firstly, to use the method of successive washes of the microbiota from the cestode's surfaces to analyze the degree of bacterial association to the tegument of the parasite. Secondly, to use a method combining the sampling of intestinal content and mucosa with the washout procedure from the mucosa to understand the real structure of the fish gut microbiota.

Results and discussion: Our results demonstrate that additional microbial community in the intestine are formed by the parasitic helminths that caused the restructuring of the microbiota in infected fish compared to those uninfected. Using the desorption method in Ringer's solution, we have demonstrated that Proteocephalus sp. cestodes possess their own microbial community which is put together from "surface" bacteria, and bacteria which are weakly and strongly associated with the tegument, bacteria obtained after treatment of the tegument with detergent, and bacteria obtained after removal of the tegument from the cestodes.

Keywords: 16S rRNA sequencing; Coregonidae; desorption; electron microscopy; microbiota; scanning and transmission electron microscopy; tegument of cestodes.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Histological dissections of whitefish intestine infected by Proteocephalus sp. (A,B) – sections were stained by Alcian Blue at pH 2.5; (C–F) by Harris’ Hematoxylin and Eosin. cs, cestode; if, intestinal folds; ic, intestinal content.
Figure 2
Figure 2
SEM and TEM observation of Proteocephalus sp. surface before (A,B,D) and after (C,E,F) Triton X-100 desorption. (A,B) SEM view of arrangement of filamentous microtriches on strobila surface. (C) SEM view of smooth surface of strobila. (D) TEM view of the tegument showing distal syncytial cytoplasm covered with microtriches and supported by basal lamina and fibrillar extracellular layer. (E) SEM view of the surface losing distal syncytial cytoplasm, note places of the connection of distal cytoplasm with sunken perikarya. (F) TEM of a portion of the tegument losing distal cytoplasm with microtriches, note basal lamina with fibrillar extracellular layer along the border of the tapeworm. bl, basal lamina; cb, cylindrical base of microtriches; dc, distal syncytial cytoplasm; ds, distal shaft of microtiches; em, extracellular matrix; fm, filamentous microtriches; mf, muscle fibers; p, pores; sm, spiniform microtriches; ss, smooth surface.
Figure 3
Figure 3
Dominant ASV at the phylum and lowest taxonomical level within the microbial communities from different segments of the digestive tract of whitefish and microbiota associated with cestodes parasitizing the intestine of “normal” C. l. pidschian.
Figure 4
Figure 4
Individual microbial community of infected “normal” C. l. pidschian and microbiota associated with cestodes parasitizing the intestine of fish.
Figure 5
Figure 5
Principal coordinates analysis (PCoA) for microbial communities of different segments of the digestive tract of uninfected and infected “normal” C. l. pidschian and cestodes parasitizing the intestine of fish.
Figure 6
Figure 6
Test effect of factor «Fish» on microbial community of cestodes using ADONIS test on Weighted UniFrac matrix.
Figure 7
Figure 7
LEfSe results presenting the identified ASV that showed significant differences in abundances between the analyzed groups. AC, anterior content; PC, posterior content; AM, anterior mucosa; PM, posterior mucosa; NA, not identified.
Figure 8
Figure 8
Schematic view of organization of different microbial communities associated with infected “normal” C. l. pidschian and the cestodes, Proteocephalus sp. parasitizing the intestine of fish.
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