Global comparison of bicosoecid Cafeteria-like flagellates from the deep ocean and surface waters, with reorganization of the family Cafeteriaceae

Schoenle, Alexandra; Hohlfeld, Manon; Rosse, Mona; Filz, Paulina; Wylezich, Claudia; Nitsche, Frank; Arndt, Hartmut

doi:10.1016/j.ejop.2019.125665

Cited by 37 publications

(32 citation statements)

References 52 publications

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“…Taxonomic groups within ciliates and other alveolates, rhizaria (radiolaria and cercozoa), amoebozoa, apusozoa, and excavates that were detected primarily in the resident population include species that are candidates in future efforts to understand the functional traits among hydrothermal vent endemic protists; many of these same groups have previously been identified as including vent endemic species (17). Heterotrophic nanoflagellate members of the stramenopile supergroup were overwhelmingly MArine STramenopiles (MAST, in cosmopolitan and resident populations) or Cafeteriaceae (primarily in the near vent bottom water samples) ( Figure 3); both are recognized as important bacterivores with a global distribution and often found in mesopelagic and deep sea surveys (35)(36)(37). MAST have also been found at higher relative sequence abundances within the Mariana Arc vent ecosystem and hydrothermally influenced water masses within Okinawa Trough (17,28).…”

Section: Protistan Grazers Exert Predation Pressure On Hydrothermal Vmentioning

confidence: 99%

Protistan grazing impacts microbial communities and carbon cycling at deep-sea hydrothermal vents

Herrera

Smith

et al. 2021

Preprint

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Microbial eukaryotes (or protists) in marine ecosystems are a link between microbial primary producers and all higher trophic levels. The rate at which heterotrophic protistan grazers consume microbial prey and recycle organic matter is an important factor that influences marine microbial food webs and carbon cycling. At deep-sea hydrothermal vents, chemosynthetic bacteria and archaea form the base of a food web that functions in the absence of sunlight, but the role of protistan grazers in these highly productive ecosystems is largely unexplored. Here, we pair grazing experiments with a molecular survey to quantify protistan grazing and to characterize the composition of vent-associated protists in low-temperature venting fluids from Gorda Ridge in the North East (NE) Pacific Ocean. Results reveal protists exert higher predation pressure at vents compared to the surrounding deep seawater environment and may account for consuming 28-62% of the daily stock of prokaryotic biomass within the hydrothermal vent food web. The vent-associated protistan community was more species rich relative to the background deep sea, and patterns in the distribution and co-occurrence of vent microbes provide additional insights into potential predator-prey interactions. Ciliates, followed by dinoflagellates, Syndiniales, rhizaria, and stramenopiles dominated the vent protist community and included bacterivorous species, species known to host symbionts, and parasites. Our findings provide an estimate of protistan grazing pressure within hydrothermal vent food webs, highlighting the role that diverse deep-sea protistan communities have in carbon cycling.

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Section: Protistan Grazers Exert Predation Pressure On Hydrothermal Vmentioning

confidence: 99%

Protistan grazing impacts microbial communities and carbon cycling at deep-sea hydrothermal vents

Herrera

Smith

et al. 2021

Preprint

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“…Phylogenetic analysis suggests that mavirus-type virophages share a common ancestry with MPEs and the related polinton-like viruses (PLVs) 9,12 . We, therefore, had previously tested the integration capacity of mavirus using the cultured protist C. burkhardae (formerly C. roenbergensis 16,17 ) and found that mavirus integrated efficiently into the nuclear host genome 10 . The resulting mavirus EVEs were transcriptionally silent unless the host cell was infected with CroV, which led to reactivation and virion formation of mavirus.…”

Section: Introductionmentioning

confidence: 99%

Virophages and retrotransposons colonize the genomes of a heterotrophic flagellate

Hackl

Duponchel

Barenhoff

et al. 2020

Preprint

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Endogenous viral elements (EVEs) are frequently found in eukaryotic genomes, yet their integration dynamics and biological functions remain largely unknown. Unlike most other eukaryotic DNA viruses, the virophage mavirus integrates efficiently into the nuclear genome of its host, the marine heterotrophic flagellate Cafeteria burkhardae. Mavirus EVEs can reactivate upon superinfection with the lytic giant virus CroV and may act as an adaptive antiviral defense system, because mavirus increases host population survival during a coinfection with CroV. However, the prevalence of endogenous virophages in natural flagellate populations has not been explored. Here we report dozens of endogenous mavirus-like elements (EMALEs) in the nuclear genomes of four C. burkhardae strains. EMALEs were typically 20 kilobase pairs long and constituted 0.7% to 1.8% of each host genome. We analyzed 33 fully assembled EMALEs that fell into two main clusters and eight types based on GC-content, nucleotide similarity, and coding potential. Inter-strain comparison showed conservation of some EMALE insertion loci, whereas the majority of integration sites were unique to a given host strain. We also describe a group of tyrosine recombinase retrotransposons, some of which exhibited a strong preference for integration into EMALEs and represent yet another layer of parasitism in this microbial system. Our findings show that virophages are common, diverse, and dynamic genome components of the marine protist C. burkhardae, which implies important eco-evolutionary roles for these enigmatic viruses.

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“…As bacterivores, Cafeteria flagellates play an important role in carbon transfer and nutrient recycling (Boenigk and Arndt, 2002;Pernthaler, 2005). Recently, many of the circulating C. roenbergensis strains have been reclassified as C. burkhardae based on 18S rDNA analysis (Schoenle et al , 2020), including the strains used in this study. Studies on Cafeteria sp.…”

Section: Introductionmentioning

confidence: 99%

Visualization of giant virus particles using BONCAT labeling and STED microscopy

Berjón-Otero

Duponchel

Hackl

et al. 2020

Preprint

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Giant DNA viruses of the phylum Nucleocytoviricota are being increasingly recognized as important regulators of natural protist populations. However, our knowledge of their infection cycles is still very limited due to a lack of cultured virus-host systems and molecular tools to study them. Here, we apply bioorthogonal noncanonical amino acid tagging (BONCAT) to pulse label the marine heterotrophic flagellate Cafeteria burkhardae during infection with the lytic giant virus CroV. In absence of CroV, we report efficient incorporation of the L-methionine analog L-azidohomoalanine (AHA) into newly synthesized proteins of the methionine prototrophic C. burkhardae. During CroV infection, AHA was predominantly found in viral proteins, and single CroV virions were imaged with stimulated emission depletion (STED) super-resolution microscopy. CroV particles incorporated AHA with 95-100% efficiency while retaining their infectivity, which makes BONCAT/STED a powerful tool to study viral replication cycles in this ecologically relevant marine bacterivore.

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Global comparison of bicosoecid Cafeteria-like flagellates from the deep ocean and surface waters, with reorganization of the family Cafeteriaceae

Cited by 37 publications

References 52 publications

Protistan grazing impacts microbial communities and carbon cycling at deep-sea hydrothermal vents

Protistan grazing impacts microbial communities and carbon cycling at deep-sea hydrothermal vents

Virophages and retrotransposons colonize the genomes of a heterotrophic flagellate

Visualization of giant virus particles using BONCAT labeling and STED microscopy

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