Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2023 Dec 19:11:e16639.
doi: 10.7717/peerj.16639. eCollection 2023.

Covariation between microeukaryotes and bacteria associated with Planorbidae snails

Camille Clerissi #  1 , Camille Huot #  2 , Anaïs Portet  3 , Benjamin Gourbal  2 , Eve Toulza  2
Affiliations

Covariation between microeukaryotes and bacteria associated with Planorbidae snails

Camille Clerissi et al. PeerJ. .

Abstract

Background: Microbial communities associated with macroorganisms might affect host physiology and homeostasis. Bacteria are well studied in this context, but the diversity of microeukaryotes, as well as covariations with bacterial communities, remains almost unknown.

Methods: To study microeukaryotic communities associated with Planorbidae snails, we developed a blocking primer to reduce amplification of host DNA during metabarcoding analyses. Analyses of alpha and beta diversities were computed to describe microeukaryotes and bacteria using metabarcoding of 18S and 16S rRNA genes, respectively.

Results: Only three phyla (Amoebozoa, Opisthokonta and Alveolata) were dominant for microeukaryotes. Bacteria were more diverse with five dominant phyla (Proteobacteria, Bacteroidetes, Tenericutes, Planctomycetes and Actinobacteria). The composition of microeukaryotes and bacteria were correlated for the Biomphalaria glabrata species, but not for Planorbarius metidjensis. Network analysis highlighted clusters of covarying taxa. Among them, several links might reflect top-down control of bacterial populations by microeukaryotes, but also possible competition between microeukaryotes having opposite distributions (Lobosa and Ichthyosporea). The role of these taxa remains unknown, but we believe that the blocking primer developed herein offers new possibilities to study the hidden diversity of microeukaryotes within snail microbiota, and to shed light on their underestimated interactions with bacteria and hosts.

Keywords: Blocking primer; Heterobranchia; Holobiont; Metabarcoding; Microbiota.

PubMed Disclaimer

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1. Microbiota samples from three snail species.
Figure 2
Figure 2. Proportion of sequences for 18SV4BP and 16SV3V4.
(A) Sequences of Planorbidae, Embryophyceae, microeukaryotes and other taxonomic groups are indicated for 18SV4BP. (B and C) Dominant phyla of snail-associated microbial communities using rarefied samples of 18SV4BP and 16SV3V4.
Figure 3
Figure 3. Distribution of dominant snail-associated microbial communities at the class level.
Clustering was computed based on class abundances using Bray-Curtis dissimilarities and Spearman’s rho correlation coefficient distances (average linkage method) for samples and taxa, respectively. The corresponding taxonomic group precedes class names (M for microeukaryotes and B for bacteria). Only classes with a relative abundance above 4% in at least one sample are shown.
Figure 4
Figure 4. Clustering of microbial communities using 18SV4BP and 16SV3V4.
Clustering were computed using Bray-Curtis dissimilarities based on OTU abundances, and the average linkage method. Each color corresponds to a snail population. The grey lines rely the same samples between 18SV4BP and 16SV3V4.
Figure 5
Figure 5. Network analyses between dominant microeukaryotes and bacteria.
The analysis was computed using the first 25 most abundant OTUs of microeukaryotes and bacteria. The corresponding taxonomic group precedes OTU numbers (M for microeukaryotes and B for bacteria). Three clusters of covarying OTUs are colored in orange, yellow and red. Red and blue lines between OTUs indicate positive or negative correlations, respectively. Line thickness highlights association strength. Dashed circles indicate the best association within each cluster.
Figure 6
Figure 6. Maximum-likelihood phylogenetic tree of microeukaryotic sequences.
The tree was rooted using B. glabrata. Numbers are ultrafast bootstraps (%) reflecting clade support of the main nodes.
Figure 7
Figure 7. Maximum-likelihood phylogenetic tree of bacterial sequences.
The tree was rooted using an archaeon. Numbers are ultrafast bootstraps (%) reflecting clade support of the main nodes.
See this image and copyright information in PMC

References

    1. Allan ERO, Tennessen JA, Sharpton TJ, Blouin MS. Allelic variation in a single genomic region alters the microbiome of the snail Biomphalaria glabrata. Journal of Heredity. 2018;109(5):604–609. doi: 10.1093/jhered/esy014. - DOI - PMC - PubMed
    1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. Journal of Molecular Biology. 1990;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. - DOI - PubMed
    1. Azam F, Fenchel T, Field J, Gray J, Meyer-Reil L, Thingstad F. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series. 1983;10:257–263. doi: 10.3354/meps010257. - DOI
    1. Baron OL, van West P, Industri B, Ponchet M, Dubreuil G, Gourbal B, Reichhart JM, Coustau C. Parental transfer of the antimicrobial protein LBP/BPI protects Biomphalaria glabrata eggs against oomycete infections. PLOS Pathogens. 2013;9(12):e1003792. doi: 10.1371/journal.ppat.1003792. - DOI - PMC - PubMed
    1. Beebee TJC, Wong AL-C. Prototheca-mediated interference competition between anuran larvae operates by resource diversion. Physiological Zoology. 1992;65(4):815–831. doi: 10.1086/physzool.65.4.30158541. - DOI

Substances