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Mollusk microbiota shift during Angiostrongylus cantonensis infection in the freshwater snail Biomphalaria glabrata and the terrestrial slug Phillocaulis soleiformis

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Abstract

In the present work, we reported for the first time the microbiome from Phyllocaulis soleiformis and Biomphalaria glabrata assessed using high-throughput DNA sequencing pre- and post-infection with the helminth parasite Angiostrongylus cantonensis. B. glabrata and P. soleiformis were experimentally infected with A. cantonensis. Fecal DNAs from control and infected groups were extracted and subjected to 16S rRNA high-throughput sequencing survey. No significant differences were found in the alpha diversity indexes in Phyllocaulis and Biomphalaria experiments independently. PCoA analysis using the unweighted UniFrac measures showed that both microbiotas behaved differently depending on the host. In Biomphalaria microbiota, control and infected groups were significantly different (p = 0.0219), while Phyllocaulis samples were not (p = 0.5190). The microbiome of P. soleiformis infected with A. cantonensis showed a significant decrease of Sphingobacterium and a substantial increase of Cellvibrio when compared to a control group. The microbiome of B. glabrata infected with A. cantonensis showed a significant decline in the abundance of Flavobacterium, Fluviicola, Nitrospira, Vogesella and an OTU belonging to the family Comamonadaceae, and a significant increase of Uliginosibacterium and an OTU belonging to the family Weeksellaceae when compared to a control group. Overall, the microbiome data reported here provided valuable information with regard to the diversity of bacterial communities that comprise the gut microbiome of gastropods. Furthermore, we report here the effect of the infection of the helminth A. cantonensis in the ratio and distribution of the fecal microbiome of the snails. Further studies are highly valuable in order to better understand those interactions by comparing different microbiome profiles and mollusk models. By now, we anticipate that ecological studies will take significant advantage of these advances, particularly concerning improving our understanding of helminth-microbiome-host interactions.

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Acknowledgments

We thank the High-Performance Computing Lab - LAD/PUCRS for allowing us access to run high-throughput sequence analyses for this study.

Funding

This work was supported by the Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico do Brasil (CNPq)—grant nos. CNPq PQ1D 307005/2014-3 (2014) and 406149/2016-0 (2016).

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Author notes

  1. Joana Borges Osório and Leandro de Mattos Pereira contributed equally to this work.

Authors and Affiliations

  1. Laboratório de Biologia Parasitária, Escola de Ciências, Pontifícia Universidade Católica do Rio Grande do Sul (PUCRS), Av. Ipiranga, 6681, Predio 12C, Porto Alegre, RS, 90060-900, Brazil

    Joana Borges Osório, Leandro de Mattos Pereira, Letícia Marconatto, Carlos Graeff-Teixeira & Alessandra Loureiro Morassutti

  2. Laboratório de Ecologia Microbiana e Molecular, Bloco E – Predio CCS, Universidade Federal do Rio de Janeiro, Av. Carlos Chagas Filho, 373, Rio de Janeiro, RJ, 21941-590, Brazil

    Leandro de Mattos Pereira & Letícia Marconatto

  3. Instituto do Petróleo e Recursos Naturais, Pontifícia Universidade Católica do Rio Grande do Sul (PUCRS), Av. Ipiranga, 6681, Predio 96J, Porto Alegre, RS, 90060-900, Brazil

    Adriana Giongo, Letícia Marconatto & Jason Mulvenna

  4. QIMR Berghofer Medical Research Institute, University of Queensland, Brisbane, Queensland, 4006, Australia

    Letícia Marconatto & Jeremy Potriquet

  5. Department of Physics, The University of Western Australia, M013, 35 Stirling Hwy, Crawley, 6009, Australia

    Letícia Marconatto & Renata Russo Frasca Candido

  6. School of Veterinary Science, The University of Queensland, Gatton, Queensland, 4343, Australia

    Letícia Marconatto & Malcolm Jones

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  1. Joana Borges Osório
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Correspondence to Alessandra Loureiro Morassutti.

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Osório, J.B., de Mattos Pereira, L., Giongo, A. et al. Mollusk microbiota shift during Angiostrongylus cantonensis infection in the freshwater snail Biomphalaria glabrata and the terrestrial slug Phillocaulis soleiformis. Parasitol Res 119, 2495–2503 (2020). https://doi.org/10.1007/s00436-020-06743-y

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