Vestigial Chloroplasts in Heterotrophic Stramenopiles Pteridomonas danica and Ciliophrys infusionum (Dictyochophyceae)

Sekiguchi, Hiroshi; Moriya, M.; Nakayama, Tsuneyoshi; Inouye, Isao

doi:10.1078/1434-4610-00094

Cited by 68 publications

(56 citation statements)

References 37 publications

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“…Actinophryids and pedinellids resemble each other in the nuclear termination of their axonemes, possessing tubular mitochondrial cristae, and having a particular type of simple extrusomes (39), which differ from the complex kinetocysts of centrohelids, desmothoracids, gymnosphaerids, and dimorphid helioflagellates (41,44,45). According to both morphological and molecular data, the pedinellids clearly belong to stramenopiles (46,47), but for the present, their relation to actinophryids remains unresolved. SSU rRNA analyses performed on stramenopiles indicate only that A. eichhornii branches within the terminal radiation of mainly autotrophic heterokont algae, which also includes the pedinellids.…”

Section: Discussionmentioning

confidence: 99%

The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes

Nikolaev

Berney²,

Fahrni³

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

225

144

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Recent molecular phylogenetic studies revealed the extraordinary diversity of single-celled eukaryotes. However, the proper assessment of this diversity and accurate reconstruction of the eukaryote phylogeny are still impeded by the lack of molecular data for some major groups of easily identifiable and cultivable protists. Among them, amoeboid eukaryotes have been notably absent from molecular phylogenies, despite their diversity, complexity, and abundance. To partly fill this phylogenetic gap, we present here combined small-subunit ribosomal RNA and actin sequence data for the three main groups of ''Heliozoa'' (Actinophryida, Centrohelida, and Desmothoracida), the heliozoan-like Sticholonche, and the radiolarian group Polycystinea. Phylogenetic analyses of our sequences demonstrate the polyphyly of heliozoans, which branch either as an independent eukaryotic lineage (Centrohelida), within stramenopiles (Actinophryida), or among cercozoans (Desmothoracida), in broad agreement with previous ultrastructure-based studies. Our data also provide solid evidence for the existence of the Rhizaria, an emerging supergroup of mainly amoeboid eukaryotes that includes desmothoracid heliozoans, all radiolarians, Sticholonche, and foraminiferans, as well as various filose and reticulose amoebae and some flagellates.

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Section: Discussionmentioning

confidence: 99%

The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes

Nikolaev

Berney²,

Fahrni³

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

225

144

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“…Interestingly, we observed that more than 90% of 16S rRNA gene sequences from Pteridomonas SAGs were closely related to a stramenopile chloroplast sequence that was neither reported in environmental sequence libraries (29,31) nor detected in other SAG 16S rRNA libraries in this study. A previous study reported that Pteridomonas danica harbors nonpigmented nonphotosynthetic plastids or vestigial chloroplasts (71); therefore, it is likely that the chloroplast sequences we recovered in 16S rRNA gene sequence libraries generated from Pteridomonas SAGs represent plastid sequences from vestigial chloroplasts. This interpretation was supported by a lack of pigmentation in Pteridomonas cells under light microscopy (data not shown).…”

Section: Isolation and Description Of Two Key Photosynthetic Protistsmentioning

confidence: 99%

Ultrastructural and Single-Cell-Level Characterization Reveals Metabolic Versatility in a Microbial Eukaryote Community from an Ice-Covered Antarctic Lake

Podar

Morgan‐Kiss

2016

Appl Environ Microbiol

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The McMurdo Dry Valleys (MCM) of southern Victoria Land, Antarctica, harbor numerous ice-covered bodies of water that provide year-round liquid water oases for isolated food webs dominated by the microbial loop. Single-cell microbial eukaryotes (protists) occupy major trophic positions within this truncated food web, ranging from primary producers (e.g., chlorophytes, haptophytes, and cryptophytes) to tertiary predators (e.g., ciliates, dinoflagellates, and choanoflagellates). To advance the understanding of MCM protist ecology and the roles of MCM protists in nutrient and energy cycling, we investigated potential metabolic strategies and microbial interactions of key MCM protists isolated from a well-described lake (Lake Bonney). Fluorescenceactivated cell sorting (FACS) of enrichment cultures, combined with single amplified genome/amplicon sequencing and fluorescence microscopy, revealed that MCM protists possess diverse potential metabolic capabilities and interactions. Two metabolically distinct bacterial clades (Flavobacteria and Methylobacteriaceae) were independently associated with two key MCM lake microalgae (Isochrysis and Chlamydomonas, respectively). We also report on the discovery of two heterotrophic nanoflagellates belonging to the Stramenopila supergroup, one of which lives as a parasite of Chlamydomonas, a dominate primary producer in the shallow, nutrient-poor layers of the lake. IMPORTANCESingle-cell eukaryotes called protists play critical roles in the cycling of organic matter in aquatic environments. In the ice-covered lakes of Antarctica, protists play key roles in the aquatic food web, providing the majority of organic carbon to the rest of the food web (photosynthetic protists) and acting as the major consumers at the top of the food web (predatory protists). In this study, we utilized a combination of techniques (microscopy, cell sorting, and genomic analysis) to describe the trophic abilities of Antarctic lake protists and their potential interactions with other microbes. Our work reveals that Antarctic lake protists rely on metabolic versatility for their energy and nutrient requirements in this unique and isolated environment. The microbial loop links the transfer of nutrients and carbon between the microorganisms of the food web and includes complex ecological interactions between microbial eukaryotes, bacteria, archaea, and viruses. Microbial activity is influenced by bottom-up (e.g., availability of nutrient and energy sources) and top-down (e.g., predation, parasitism, and viral lysis) controls, as well as microbe-microbe interactions (e.g., bacterial consortia). Interaction partnerships between microorganisms lead to combinations of win, loss, or neutral outcomes for each microbial partner. Parasitism and predation are examples of win-loss outcomes (1), while mutualistic interactions within biofilms and syntrophic interactions (cross-feeding of metabolic products between two species) between an alga and a heterotrophic bacterium are examples of win-win partnerships (2). ...

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“…As they have lost photosynthesis, one would expect all the genes related to this process to be gone as well, and in several cases they are (Wilson et al 1996;de Koning & Keeling 2006). In other cases, however, some of the genes that have been retained are of interest given the absence of photosynthesis, such as ATP synthase genes in Prototheca or rubisco subunits in nonphotosynthetic heterokonts and plants (Wolfe & dePamphilis 1997;Knauf & Hachtel 2002;Sekiguchi et al 2002;McNeal et al 2007;Barrett & Freudenstein 2008;Krause 2008). …”

Section: Plastid Loss and Cryptic Plastidsmentioning

confidence: 99%

The endosymbiotic origin, diversification and fate of plastids

Keeling

2010

Phil. Trans. R. Soc. B

583

483

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Plastids and mitochondria each arose from a single endosymbiotic event and share many similarities in how they were reduced and integrated with their host. However, the subsequent evolution of the two organelles could hardly be more different: mitochondria are a stable fixture of eukaryotic cells that are neither lost nor shuffled between lineages, whereas plastid evolution has been a complex mix of movement, loss and replacement. Molecular data from the past decade have substantially untangled this complex history, and we now know that plastids are derived from a single endosymbiotic event in the ancestor of glaucophytes, red algae and green algae (including plants). The plastids of both red algae and green algae were subsequently transferred to other lineages by secondary endosymbiosis. Green algal plastids were taken up by euglenids and chlorarachniophytes, as well as one small group of dinoflagellates. Red algae appear to have been taken up only once, giving rise to a diverse group called chromalveolates. Additional layers of complexity come from plastid loss, which has happened at least once and probably many times, and replacement. Plastid loss is difficult to prove, and cryptic, non-photosynthetic plastids are being found in many non-photosynthetic lineages. In other cases, photosynthetic lineages are now understood to have evolved from ancestors with a plastid of different origin, so an ancestral plastid has been replaced with a new one. Such replacement has taken place in several dinoflagellates (by tertiary endosymbiosis with other chromalveolates or serial secondary endosymbiosis with a green alga), and apparently also in two rhizarian lineages: chlorarachniophytes and Paulinella (which appear to have evolved from chromalveolate ancestors). The many twists and turns of plastid evolution each represent major evolutionary transitions, and each offers a glimpse into how genomes evolve and how cells integrate through gene transfers and protein trafficking.

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Vestigial Chloroplasts in Heterotrophic Stramenopiles Pteridomonas danica and Ciliophrys infusionum (Dictyochophyceae)

Cited by 68 publications

References 37 publications

The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes

The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes

Ultrastructural and Single-Cell-Level Characterization Reveals Metabolic Versatility in a Microbial Eukaryote Community from an Ice-Covered Antarctic Lake

The endosymbiotic origin, diversification and fate of plastids

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