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

Holt, Corey C.; Boscaro, Vittorio; Steenkiste, Niels Van; Herranz, María; Mathur, Varsha; Irwin, Nicholas A. T.; Buckholtz, Gracy; Leander, Brian S.; Keeling, Patrick J.

doi:10.1186/s40168-022-01363-3

Cited by 15 publications

(10 citation statements)

References 117 publications

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“…Generally, the microbiome of an invertebrate constitutes a diverse set of organisms that can serve as hosts for very different viruses. Although the bacterial part of the microbiome can be ignored in this context, because phages have been excluded from the analysis, the eukaryotic fraction is nowhere near negligible in invertebrate microbiomes ( 91 ). The common occurrence of these symbioses could have further contributed to the reported abundance of protist-infecting NCLDVs.…”

Section: Resultsmentioning

confidence: 99%

Unveiling the hidden viromes across the animal tree of life: insights from a taxonomic classification pipeline applied to invertebrates of 31 metazoan phyla

Alfonso,

Butković,

Fernández

et al. 2024

mSystems

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Invertebrates constitute the majority of animal species on Earth, including most disease-causing agents or vectors, with more diverse viromes when compared to vertebrates. Recent advancements in high-throughput sequencing have significantly expanded our understanding of invertebrate viruses, yet this knowledge remains biased toward a few well-studied animal lineages. In this study, we analyze invertebrate DNA and RNA viromes for 31 phyla using 417 publicly available RNA-Seq data sets from diverse environments in the marine-terrestrial and marine-freshwater gradients. This study aims to (i) estimate virome compositions at the family level for the first time across the animal tree of life, including the first exploration of the virome in several phyla, (ii) quantify the diversity of invertebrate viromes and characterize the structure of invertebrate-virus infection networks, and (iii) investigate host phylum and habitat influence on virome differences. Results showed that a set of few viral families of eukaryotes, comprising Retroviridae , Flaviviridae , and several families of giant DNA viruses, were ubiquitous and highly abundant. Nevertheless, some differences emerged between phyla, revealing for instance a less diverse virome in Ctenophora compared to the other animal phyla. Compositional analysis of the viromes showed that the host phylum explained over five times more variance in composition than its habitat. Moreover, significant similarities were observed between the viromes of some phylogenetically related phyla, which could highlight the influence of co-evolution in shaping invertebrate viromes. IMPORTANCE This study significantly enhances our understanding of the global animal virome by characterizing the viromes of previously unexamined invertebrate lineages from a large number of animal phyla. It showcases the great diversity of viromes within each phylum and investigates the role of habitat shaping animal viral communities. Furthermore, our research identifies dominant virus families in invertebrates and distinguishes phyla with analogous viromes. This study sets the road toward a deeper understanding of the virome across the animal tree of life.

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Section: Resultsmentioning

confidence: 99%

Unveiling the hidden viromes across the animal tree of life: insights from a taxonomic classification pipeline applied to invertebrates of 31 metazoan phyla

Alfonso,

Butković,

Fernández

et al. 2024

mSystems

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“…In addition, zoosporic parasites likely play a significant role in maintaining genetic polymorphism and biodiversity in host populations and regulating phytoplankton succession. They can infect several types of plankton including protozoan, such as dinoflagellates or ciliates, and metazoans, such as crustaceans and copepods as endoparasites ( 47 ). Because of their short generation times and abundant progeny, zoosporic parasitoids exert important top-down control that significantly influences the entire aquatic food webs, especially phytoplankton population dynamics.…”

Section: Discussionmentioning

confidence: 99%

Insight into planktonic protistan and fungal communities across the nutrient-depleted environment of the South Pacific Subtropical Gyre

Kajan,

Fuchs,

Orlić

2024

Microbiol Spectr

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Our findings carry important implications for understanding the distribution patterns of the previously unrecognized occurrence of parasitic protists and functionally diverse fungi in the nutrient-limited South Pacific Gyre. In particular, our study reveals a significant presence of parasitic Syndiniales, predominantly abundant in the upper 300 m of the aphotic zone in the gyre, and a distinct presence of fungal communities in the aphotic zone at the central part of the gyre. These findings strongly suggest that these communities play a substantial role in yet insufficiently described microbial food web. Moreover, our research enhances our understanding of their contribution to the dynamics of the food webs in oligotrophic gyres and is valuable for projecting the ecological consequences of future climate warming.

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“…The marine alveolates (MALVs) are an elusive group of microbial eukaryotes first discovered through amplicon surveys of environmental rRNA 1,2 , and since found to consistently dominate eukaryotic metabarcoding surveys in global oceans 3,4,5,6,7 . Virtually all MALVs are known only from these rRNA SSU gene fragments, which have been phylogenetically linked to a handful of described parasites related to dinoflagellates 1,9,10,11 .…”

Section: Mainmentioning

confidence: 99%

Multiple parallel origins of parasitic Marine Alveolates

Holt

Hehenberger

Tikhonenkov

et al. 2023

Preprint

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Microbial eukaryotes are important components of marine ecosystems, and the Marine Alveolates (MALVs) are consistently one of the most abundant and diverse groups of eukaryotes in global environmental sequencing surveys. Relatives of the dinoflagellates, MALVs are thought to be parasites of animals and other protists but the absence of data beyond ribosomal RNA gene sequences from all but two species means much of their biology and evolution remain unknown. Here we show that MALVs evolved independently from two distinct, free-living ancestors and that parasitism evolved twice, in parallel, prior to the divergence of the core dinoflagellates. Phylogenomics shows one subgroup (MALV II and IV, or Syndiniales) to be related to a novel lineage of free-living, eukaryovorous predators, the eleftherids, while the other (MALV I, now the Ichthyodiniales) is related to Oxyrrhis marina. Reconstructing the evolution of photosynthesis, plastids, and parasitism in early-diverging dinoflagellates show a number of parallels with the evolution of their sister group, the parasitic apicomplexans. In both groups, similar forms of parasitism evolved multiple times, photosynthesis was lost many times, and the plastid organelle was lost infrequently, leaving no trace in the genome that they ever existed.

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

Cited by 15 publications

References 117 publications

Unveiling the hidden viromes across the animal tree of life: insights from a taxonomic classification pipeline applied to invertebrates of 31 metazoan phyla

Unveiling the hidden viromes across the animal tree of life: insights from a taxonomic classification pipeline applied to invertebrates of 31 metazoan phyla

Insight into planktonic protistan and fungal communities across the nutrient-depleted environment of the South Pacific Subtropical Gyre

Multiple parallel origins of parasitic Marine Alveolates

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