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

Elena N Kashinskaya; Evgeniy P Simonov; Larisa G Poddubnaya; Pavel G Vlasenko; Anastasiya V Shokurova; Aleksey N Parshukov; Karl B Andree; Mikhail M Solovyev

doi:10.3389/fmicb.2023.1090899

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

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

Authors

Elena N Kashinskaya^{1

2}, Evgeniy P Simonov^{1

2}, Larisa G Poddubnaya³, Pavel G Vlasenko^{1

2}, Anastasiya V Shokurova^{1

2}, Aleksey N Parshukov⁴, Karl B Andree⁵, Mikhail M Solovyev^{1

2

6}

Affiliations

¹ Institute of Systematics and Ecology of Animals, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia.
² A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, Moscow, Russia.
³ Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, Yaroslavl Region, Russia.
⁴ Institute of Biology of the Karelian Research Centre, Russian Academy of Sciences, Petrozavodsk, Russia.
⁵ Institut de Recerca i Tecnologìa Agroalimentaries (IRTA), Sant Carles de la Ràpita, Spain.
⁶ Tomsk State University, Biological Institute, Tomsk, Russia.

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.