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other·microbiology, parasitology, ecology, fisheries science, gastroenterology·PMC10043260

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

Frontiers in Microbiology · 8 authors, 6 centres

AI SUMMARY

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POPULATIONSympatric pair of whitefish Coregonus lavaretus complex: 'dwarf' planktivorous C. l. pravdinellus (TL 158.8 ± 2.6 mm, n=14, all infected) and 'normal' benthivorous C. l. pidschian (uninfected TL 252.2 ± 6.4 mm, n=13; infected TL 241.3 ± 4.3 mm, n=9) from Teletskoye Lake, Russia.

INTERVENTIONInfection by Proteocephalus sp. cestodes in the intestine; comparison of infected vs. uninfected fish and different feeding forms.

COMPARISONGut microbiota (mucosa, content, washout) of infected vs. uninfected 'normal' whitefish; 'dwarf' (all infected) vs. 'normal' whitefish; cestode fractions (D0–D7) from serial desorption vs. host gut microbiota.

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TL;DR

This study characterizes the gut microbiota of two sympatric whitefish forms (planktivorous 'dwarf' and benthivorous 'normal') and the associated microbiota of Proteocephalus sp. cestodes infecting their intestines. Using a novel desorption method with 16S rRNA sequencing, the authors demonstrate that cestodes harbor their own distinct microbial communities layered across the tegument, and that parasite infection significantly restructures the host gut microbiota. The findings highlight that parasitic helminths create additional ecological niches in the fish gut, increasing overall microbial diversity and underscoring the need to account for parasite infection in microbiome studies.

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**Background:** The impact of parasites on host gut microbiota is well documented, but the role of parasite-host relationships in shaping microbiota is poorly understood. This study investigated how trophic behavior and resulting parasitism influence microbiome structure in a sympatric pair of whitefish (Coregonus lavaretus complex) from Teletskoye Lake, Siberia. The 'dwarf' planktivorous form C. l. pravdinellus (100% prevalence of Proteocephalus sp.) and the 'normal' benthivorous form C. l. pidschian (45% prevalence) provided a natural model of infected and uninfected fish with different feeding habits.

**Methods:** In August 2019, fish were collected from the north part of Teletskoye Lake (51.79°N; 87.30°E). The digestive tract was divided into stomach, anterior intestine, and posterior intestine. Content, mucosa scrapings, and washout (sterile 0.9% NaCl) samples were collected from each segment. For cestodes, a novel desorption method was applied: after removal from the intestine, cestodes were placed in Ringer's solution (fraction D0), then subjected to sequential vortexing (15 s at 900 rpm for D1; 15 min at 900 rpm for D2–D5), treatment with 0.2% Triton X-100 detergent (D6), and finally removal of the tegument (D7). A total of 153 cestode samples were collected. DNA was extracted and the V3-V4 region of 16S rRNA was sequenced on Illumina MiSeq (2×300 bp paired-end). Data were processed with DADA2 (ASVs at 100% identity), taxonomy assigned with IDTAXA using SILVA SSU r138. Alpha-diversity (ASV, Shannon, Simpson) was compared with Kruskal-Wallis and Dunn's tests. Beta-diversity was assessed with PERMANOVA (Bray-Curtis, 10,000 permutations) and visualized with PCoA. LEfSe identified biomarkers (alpha=0.01, LDA threshold=4.0). SEM and TEM confirmed tegument structure before and after desorption.

**Key Results:** 28S rRNA analysis confirmed all cestodes were the same Proteocephalus species. SEM/TEM showed dense filamentous microtriches on the tegument that were completely removed after Triton X-100 treatment, leaving only the basal lamina. Alpha-diversity: In infected 'normal' whitefish, the highest richness was in posterior intestine content (ASV 602.6 ± 124.9, Shannon 5.1 ± 0.3) and lowest in anterior mucosa (ASV 37.8 ± 7.1, Shannon 2.3 ± 0.3). In uninfected 'normal' whitefish, highest was in anterior content (ASV 312.2 ± 59.7, Shannon 4.0 ± 0.4) and lowest in posterior washout (ASV 28.3 ± 3.8, Shannon 1.9 ± 0.2). In 'dwarf' whitefish, highest was in posterior content (ASV 144.8 ± 22.4, Shannon 2.5 ± 0.3) and lowest in anterior mucosa (ASV 26.6 ± 4.3, Shannon 1.3 ± 0.1). For cestode fractions, D0 had the highest richness (ASV 218.1 ± 91.6, Shannon 2.8 ± 0.6), significantly different from D1–D6 (Dunn's test, p<0.05). D7 (ASV 51.1 ± 2.3, Shannon 2.2 ± 0.2) was significantly different from D2–D6. Beta-diversity: Significant differences were found between infected and uninfected 'normal' whitefish for stomach mucosa and anterior/posterior content (ADONIS, p<0.05). Cestode fractions D0, D6, and D7 were significantly different from all other fractions (p<0.05). The factor 'Fish' (individual host) significantly affected cestode microbiota (ADONIS, p<0.05), indicating host-specific microbial communities. Taxonomic composition: In infected 'normal' whitefish, Proteobacteria dominated (40.3–66.5% in intestine). In uninfected fish, Aeromonas was more abundant (15.8–39.5% in intestine). In 'dwarf' whitefish, Firmicutes dominated (up to 87.0%), with Clostridium sensu stricto 1 (35.8 ± 12.0% in stomach mucosa) and Mycoplasma (87.0 ± 3.4% in anterior mucosa). Cestode fractions were dominated by Proteobacteria (56.8–68.0%) and Firmicutes (20.4–40.2%). LEfSe identified Sphingobium as a biomarker for D1 (LDA=4.95, p=5.10E-03), Mycoplasma for D2 (LDA=5.31, p=2.80E-03), Acinetobacter and Allorhizobium for D6 (LDA=5.10, p=1.40E-07; LDA=4.75, p=4.10E-10), and Comamonas, Cupriavidus, Stenotrophomonas, Thermus for D7 (LDA=4.92, p=2.49E-08; LDA=4.02, p=8.00E-07; LDA=4.35, p=1.30E-10; LDA=4.31, p=9.00E-08).

**Clinical Implications:** This study demonstrates that parasitic helminths (cestodes) in fish intestines harbor their own distinct, layered microbial communities that differ from the host gut microbiota. Cestode infection significantly restructures the host gut microbial composition, notably increasing Mycoplasma abundance and reducing Aeromonas in infected 'normal' whitefish. The findings underscore that parasites are not merely passengers but active ecological niche modifiers that increase overall microbial diversity in the gut ecosystem. The novel desorption methodology provides a framework for disentangling host, parasite, and microbial interactions. These results have implications for any vertebrate microbiome study where parasitic infections are common—ignoring this factor may lead to biased interpretations of 'normal' microbiota. The increased bacterial diversity associated with parasite infection may help host populations resist environmental disturbances, though further research is needed.

PICO

PPOPULATION

Sympatric pair of whitefish Coregonus lavaretus complex: 'dwarf' planktivorous C. l. pravdinellus (TL 158.8 ± 2.6 mm, n=14, all infected) and 'normal' benthivorous C. l. pidschian (uninfected TL 252.2 ± 6.4 mm, n=13; infected TL 241.3 ± 4.3 mm, n=9) from Teletskoye Lake, Russia.

IINTERVENTION

Infection by Proteocephalus sp. cestodes in the intestine; comparison of infected vs. uninfected fish and different feeding forms.

OOUTCOME

Alpha-diversity (ASV, Shannon, Simpson), beta-diversity (Bray-Curtis, PERMANOVA), taxonomic composition at phylum and genus level, LEfSe biomarkers. Cestode infection significantly affected microbial communities of stomach and intestinal content in 'normal' whitefish (ADONIS, p<0.05). Cestodes possessed distinct microbial communities with layered organization across tegument.

STUDY TYPE

other

SPECIALTY

microbiology

SUMMARISED BY

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FIDELITY CHECK

100% · A

ORIGINAL PAPER

PMC10043260

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

Frontiers in Microbiology

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ABSTRACT

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

CITATION EXPORT

Elena N Kashinskaya, Evgeniy P Simonov, Larisa G Poddubnaya et al.. Trophic diversification and parasitic invasion as ecological niche modulators for gut microbiota of whitefish. Frontiers in Microbiology. (2023). https://doi.org/10.3389/fmicb.2023.1090899

AUTHORS

8 · 6 CENTRES

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

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