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

Kashinskaya, E. N.; Simonov, Evgeniy; Poddubnaya, Larisa G.; Vlasenko, Pavel; Shokurova, Anastasiya V.; Parshukov, Aleksey; Andrée, Karl B.; Solovyev, Mikhail

doi:10.3389/fmicb.2023.1090899

Cited by 6 publications

(2 citation statements)

References 49 publications

(72 reference statements)

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“…Moreover, there is a lack of literature on the relationship between intestinal parasites and the intestinal microbiome of fish. Few studies have presented discordant results regarding the impact of parasites on fish intestinal microbiota biodiversity ( Scholz et al., 2011 ; Oros et al., 2015 ; Vasemägi et al., 2017 ; Kashinskaya et al., 2023 ). This motivated us to develop an infection model to study intestinal parasite and microbiota interactions on fish health, using C. punctata as a fish model.…”

Section: Discussionmentioning

confidence: 99%

Deciphering the impact of endoparasitic infection on immune response and gut microbial composition of Channa punctata

Kumar,

Roy,

Parida

et al. 2024

Front. Cell. Infect. Microbiol.

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Intestinal parasitic infections caused by helminths are globally distributed and are a major cause of morbidity worldwide. Parasites may modulate the virulence, gut microbiota diversity and host responses during infection. Despite numerous works, little is known about the complex interaction between parasites and the gut microbiota. In the present study, the complex interplay between parasites and the gut microbiota was investigated. A total of 12 bacterial strains across four major families, including Enterobacteriaceae, Morganellaceae, Flavobacteriaceae, and Pseudomonadaceae, were isolated from Channa punctata, infected with the nematode species Aporcella sp., Axonchium sp., Tylencholaimus mirabilis, and Dioctophyme renale. The findings revealed that nematode infection shaped the fish gut bacterial microbiota and significantly affected their virulence levels. Nematode-infected fish bacterial isolates are more likely to be pathogenic, with elevated hemolytic activity and biofilm formation, causing high fish mortality. In contrast, isolates recovered further from non-parasitised C. punctata were observed to be non-pathogenic and had negligible hemolytic activity and biofilm formation. Antibiogram analysis of the bacterial isolates revealed a disproportionately high percentage of bacteria that were either marginally or multidrug resistant, suggesting that parasitic infection-induced stress modulates the gut microenvironment and enables colonization by antibiotic-resistant strains. This isolation-based study provides an avenue to unravel the influence of parasitic infection on gut bacterial characteristics, which is valuable for understanding the infection mechanism and designing further studies aimed at optimizing treatment strategies. In addition, the cultured isolates can supplement future gut microbiome studies by providing wet lab specimens to compare (meta)genomic information discovered within the gut microenvironment of fish.

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Section: Discussionmentioning

confidence: 99%

Deciphering the impact of endoparasitic infection on immune response and gut microbial composition of Channa punctata

Kumar,

Roy,

Parida

et al. 2024

Front. Cell. Infect. Microbiol.

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“…Gut dysbiosis is frequently associated with helminth infections [12][13][14] , and in some systems, the gut microbiota composition directly promotes or inhibits helminth colonisation or reproduction [15][16][17] . Furthermore, some parasitic helminths have been shown to carry an internal microbiota 13,[18][19][20] , including essential endosymbionts 21 . Helminths and other parasites may also act as vectors, introducing novel, potentially pathogenic, microbes to the host animal [22][23][24] .…”

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confidence: 99%

Host-gut microbiota interactions shape parasite infections in farmed Atlantic salmon

Brealey¹,

Kodama²,

Rasmussen³

et al. 2023

Preprint

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Animals and their associated microbiota share long evolutionary histories. Both host genotype and associated microbiota influence phenotypes such as growth and disease resilience. We applied a hologenomic approach to explore the relationship between host and microbiota in shaping lifetime growth and parasitic cestode infection in farmed Atlantic salmon. Genomes, transcriptomes, metabolomes and metagenomes were generated from the guts of 460 harvest-aged salmon, 82% of which were naturally infected with an intestinal cestode. One salmonid-specific Mycoplasma dominated the gut microbiota of uninfected salmon. However, the microbiota was perturbed in smaller, parasitised fish, with increased abundance of Vibrionaceae and other Mycoplasma species previously linked to the cestode microbiota. The cestode-associated Mycoplasma carry more virulence-associated genes than the salmonid Mycoplasma. Colonisation by one cestode-associated Mycoplasma was associated with a region of the salmon genome encoding several long noncoding RNA genes previously associated with host control of intestinal microbiota. Integrating the multiple omic datasets revealed coordinated changes in the salmon gut transcriptome and metabolome that correlated with shifts in the microbiota of smaller, parasitised fish. Our results suggest that cestode infections introduce new microbes and trigger host responses, altering the gut microbiota with increases in potentially pathogenic microbes. Establishment of these microbes is partially shaped by the genetic background of the host. Our study highlights the value of a hologenomic approach for gaining an in-depth understanding of trilateral interactions among host, microbiota and parasite.

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Host–gut microbiota interactions shape parasite infections in farmed Atlantic salmon

Brealey,

Kodama,

Rasmussen

et al. 2024

mSystems

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Animals and their associated microbiota share long evolutionary histories. However, it is not always clear how host genotype and microbiota interact to affect phenotype. We applied a hologenomic approach to explore how host–microbiota interactions shape lifetime growth and parasite infection in farmed Atlantic salmon ( Salmo salar ). Multi-omics data sets were generated from the guts of 460 salmon, 82% of which were naturally infected with an intestinal cestode. A single Mycoplasma bacterial strain, MAG01, dominated the gut metagenome of large, non-parasitized fish, consistent with previous studies showing high levels of Mycoplasma in the gut microbiota of healthy salmon. While small and/or parasitized salmon also had high abundance of MAG01, we observed increased alpha diversity in these individuals, driven by increased frequency of low-abundance Vibrionaceae and other Mycoplasma species that carried known virulence genes. Colonization by one of these cestode-associated Mycoplasma strains was associated with host individual genomic variation in long non-coding RNAs. Integrating the multi-omic data sets revealed coordinated changes in the salmon gut mRNA transcriptome and metabolome that correlated with shifts in the microbiota of smaller, parasitized fish. Our results suggest that the gut microbiota of small and/or parasitized fish is in a state of dysbiosis that partly depends on the host genotype, highlighting the value of using a hologenomic approach to incorporate the microbiota into the study of host–parasite dynamics. IMPORTANCE Studying host–microbiota interactions through the perspective of the hologenome is gaining interest across all life sciences. Intestinal parasite infections are a huge burden on human and animal health; however, there are few studies investigating the role of the hologenome during parasite infections. We address this gap in the largest multi-omics fish microbiota study to date using natural cestode infection of farmed Atlantic salmon. We find a clear association between cestode infection, salmon lifetime growth, and perturbation of the salmon gut microbiota. Furthermore, we provide the first evidence that the genetic background of the host may partly determine how the gut microbiota changes during parasite-associated dysbiosis. Our study therefore highlights the value of a hologenomic approach for gaining a more in-depth understanding of parasitism.

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

Cited by 6 publications

References 49 publications

Deciphering the impact of endoparasitic infection on immune response and gut microbial composition of Channa punctata

Deciphering the impact of endoparasitic infection on immune response and gut microbial composition of Channa punctata

Host-gut microbiota interactions shape parasite infections in farmed Atlantic salmon

Host–gut microbiota interactions shape parasite infections in farmed Atlantic salmon

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