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. 2022 Sep 30;10(1):161.
doi: 10.1186/s40168-022-01363-3.

Microscopic marine invertebrates are reservoirs for cryptic and diverse protists and fungi

Corey C Holt  1   2 , Vittorio Boscaro  3   4 , Niels W L Van Steenkiste  3   4   5 , Maria Herranz  3   4   5   6 , Varsha Mathur  3 , Nicholas A T Irwin  3 , Gracy Buckholtz  3 , Brian S Leander  3   5 , Patrick J Keeling  7
Affiliations

Microscopic marine invertebrates are reservoirs for cryptic and diverse protists and fungi

Corey C Holt et al. Microbiome. .

Abstract

Background: Microbial symbioses in marine invertebrates are commonplace. However, characterizations of invertebrate microbiomes are vastly outnumbered by those of vertebrates. Protists and fungi run the gamut of symbiosis, yet eukaryotic microbiome sequencing is rarely undertaken, with much of the focus on bacteria. To explore the importance of microscopic marine invertebrates as potential symbiont reservoirs, we used a phylogenetic-focused approach to analyze the host-associated eukaryotic microbiomes of 220 animal specimens spanning nine different animal phyla.

Results: Our data expanded the traditional host range of several microbial taxa and identified numerous undescribed lineages. A lack of comparable reference sequences resulted in several cryptic clades within the Apicomplexa and Ciliophora and emphasized the potential for microbial invertebrates to harbor novel protistan and fungal diversity.

Conclusions: Microscopic marine invertebrates, spanning a wide range of animal phyla, host various protist and fungal sequences and may therefore serve as a useful resource in the detection and characterization of undescribed symbioses. Video Abstract.

Keywords: 18S; ASV; Aquatic; Host-associated; Invertebrate; Microbiota; Symbiont.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Overview of more than 200 specimens and visual evidence of symbiosis. a Sankey diagram showing the distribution of specimen locations, habitats, and phyla, with the number of specimens accompanying each factor. b Photos of representative specimens from each invertebrate phylum. c Unknown Apicomplexa shown in a Platyhelminthes specimen belonging to the family Koinocystididae. d Epibiont ciliates of the genus Rhabdostyla (black arrows) on an unknown species of a Syllis polychaete (Annelida). e Potential fungal structures on the dorsal side of a harpacticoid copepod. Image darkened to aid visibility
Fig. 2
Fig. 2
Apicomplexa prevalence and diversity. Maximum-likelihood phylogeny of all Apicomplexa ASVs, reference sequences, and BLAST hits using the GTR+F+R7 substitution model. Individual ASVs are indicated by white rectangles in the gray ring. Accompanying dots reflect the presence in each host phylum (colored accordingly). Black bars in the outer ring reflect the number of specimens associated with each ASV (on a log scale). Nodes are labeled to show UltraFast bootstrap support and taxonomic clades are annotated by color. a Percentage of individuals with at least one ASV in the tree. b Absolute number of distinct ASVs. c–g Highlighted lineages discussed in the text
Fig. 3
Fig. 3
Environmental and host-associated ciliate lineages. Maximum-likelihood phylogeny of all Ciliophora ASVs, reference sequences and best BLAST hits using the GTR+F+R7 substitution model. Individual ASVs indicated by white rectangles in a gray ring. Accompanying dots reflect the presence in each host phylum (colored accordingly). Black bars in the outer ring reflect the number of specimens associated with each ASV (on a log scale). Nodes are labeled to show UltraFast bootstrap support and taxonomic clades are annotated by color. Outer red clade labels show host-associated taxa (single line) and epibiotic symbionts (double line). a Percentage of individuals with at least one ASV in the tree. b Absolute number of distinct ASVs. c–e Highlighted lineages discussed in the text
Fig. 4
Fig. 4
Evidence of fungal ASVs in marine invertebrates. Maximum-likelihood phylogeny of all Fungi ASVs, reference sequences and best BLAST hits using the GTR+F+R7 substitution model. Individual ASVs indicated by white rectangles in a gray ring. Accompanying dots reflect the presence in each host phylum (colored accordingly). Black bars in the outer ring reflect the number of specimens associated with each ASV (on a log scale). Nodes are labeled to show UltraFast bootstrap support and taxonomic clades are annotated by color. a Percentage of individuals with at least one ASV in the tree. b Absolute number of distinct ASVs. c–e Highlighted lineages discussed in the text
Fig. 5
Fig. 5
Other invertebrate symbiont taxa. Maximum-likelihood phylogeny of a marine alveolates (MALVs) and Perkinsea and d Stramenopiles ASVs, reference sequences and best BLAST hits using the GTR+F+R7 substitution model. Individual ASVs indicated by white rectangles in a gray ring. Accompanying dots reflect the presence in each host phylum (colored accordingly). Black bars in the outer ring reflect the number of specimens associated with each ASV (on a log scale). Nodes are labeled to show UltraFast bootstrap support and taxonomic clades are annotated by color. b, c, e, f Highlight lineages discussed in the text
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