Extrusomes in Ciliates: Diversification, Distribution, and Phylogenetic Implications

Rosati, Giovanna; Modeo, Letizia

doi:10.1111/j.1550-7408.2003.tb00260.x

Cited by 99 publications

(84 citation statements)

References 137 publications

(214 reference statements)

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“…Both of these phenomena have also been observed within the DCGs of unicellular ciliates (3,14). In addition, ciliate DCGs demonstrate another degree of subtlety in DCG formation because the granule cores in many of these organisms are divided into distinct domains (25). The domain organization indicates that DCG proteins in these cells can segregate from one another even as they are sorted to the same vesicular destination.…”

mentioning

confidence: 83%

Independent Transport and Sorting of Functionally Distinct Protein Families in Tetrahymena thermophila Dense Core Secretory Granules

2009

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Dense core granules (DCGs) in Tetrahymena thermophila contain two protein classes. Proteins in the first class, called granule lattice (Grl), coassemble to form a crystalline lattice within the granule lumen. Lattice expansion acts as a propulsive mechanism during DCG release, and Grl proteins are essential for efficient exocytosis. The second protein class, defined by a C-terminal ␤/␥-crystallin domain, is poorly understood. Here, we have analyzed the function and sorting of Grt1p (granule tip), which was previously identified as an abundant protein in this family. Cells lacking all copies of GRT1, together with the closely related GRT2, accumulate wild-type levels of docked DCGs. Unlike cells disrupted in any of the major GRL genes, ⌬GRT1 ⌬GRT2 cells show no defect in secretion, indicating that neither exocytic fusion nor core expansion depends on GRT1. These results suggest that Grl protein sorting to DCGs is independent of Grt proteins. Consistent with this, the granule core lattice in ⌬GRT1 ⌬GRT2 cells appears identical to that in wild-type cells by electron microscopy, and the only biochemical component visibly absent is Grt1p itself. Moreover, gel filtration showed that Grl and Grt proteins in cell homogenates exist in nonoverlapping complexes, and affinity-isolated Grt1p complexes do not contain Grl proteins. These data demonstrate that two major classes of proteins in Tetrahymena DCGs are likely to be independently transported during DCG biosynthesis and play distinct roles in granule function. The role of Grt1p may primarily be postexocytic; consistent with this idea, DCG contents from ⌬GRT1 ⌬GRT2 cells appear less adhesive than those from the wild type.

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confidence: 83%

Independent Transport and Sorting of Functionally Distinct Protein Families in Tetrahymena thermophila Dense Core Secretory Granules

2009

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“…Terminology is according to Foissner and Agatha (1999), Jankowski (1964b), Lynn (2008 and Rosati and Modeo (2003). We define the ventral side of the cell as that surface on which the terminus of the adoral zone (and the cytostome) is at the right margin.…”

Section: Terminologymentioning

confidence: 99%

“…In the following discussion, we consider protrichocysts, mucocysts and cortical granules as synonymous (Rosati and Modeo 2003). Admittedly, relatively little is known about their prevalence, structure and function in metopid ciliates.…”

Section: Cortical Granulation In Metopidsmentioning

confidence: 99%

Morphologic and molecular description of Metopus fuscus Kahl from North America and new rDNA sequences from seven metopids (Armophorea, Metopidae)

Bourland

Wendell

Hampikian

2014

European Journal of Protistology

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Most species in the large ciliate genus Metopus Claparède & Lachmann, 1858 lack detailed descriptions based on modern morphologic and molecular methods. This lack of data for the vast majority of species hampers application of a morphospecies approach to the taxonomy of Metopus and other armophorids. In this report we redescribe the large species, Metopus fuscus Kahl, 1927 based on in vivo observation, silver impregnation, scanning electron microscopy, and single-cell 18S rDNA sequencing of a freshwater North American (Idaho) population. Metopus fuscus invariably has a perinuclear envelope of endosymbiotic bacteria not found in other species. Unlike the original description of a single row of coarse granules between ciliary rows, the Idaho population has five loose rows of small interkinetal granules. We discuss the possible importance of this character in metopids. We also provide a phylogenetic analysis including setosus form a fully supported clade, challenging previous morphospecies groupings. We discuss some ambiguities of armophorid morphologic terminology in the earlier literature. Our phylogenetic analysis of Idaho metopids indicates that the genera Metopus and Brachonella are both nonmonophyletic.

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“…Nevertheless, in M. rubrum, the anterior tentacles have been shown to capture a prey item following detection of a hydromechanical signal, similar to the mechanism observed in M. pulex (Jakobsen et al 2006), a closely related heterotrophic ciliate. The anterior tentacles are associated with a number of extrusomes (Lindholm et al 1988), which often secrete cell contents or mucilaginous material (Rosati & Modeo 2003). Once captured, cryptophytes are carried toward a rudimentary cytostome at the oral end of the ciliate, where they are then engulfed in a clear pouch-like area one at a time and assimilated in a timeframe of ~90 s (Yih et al 2004).…”

Section: Resale or Republication Not Permitted Without Written Consenmentioning

confidence: 99%

Associations between Mesodinium rubrum and cryptophyte algae in the Columbia River estuary

Peterson¹,

Golda

Garcia

et al. 2013

Aquat. Microb. Ecol.

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Recurring blooms of the photosynthetic ciliate Mesodinium rubrum (= Myrionecta rubra) are observed each summer in the Columbia River estuary. Although cultured isolates of M. rubrum have been shown to consume cryptophyte prey during growth, the feeding behavior of M. rubrum in the field is poorly known. In the present study, a 3 mo time series of observations from a locale of putative bloom formation (Ilwaco harbor in Baker Bay, WA) showed that cryptophytes were present at relatively high abundance prior to and during M. rubrum blooms and declined with M. rubrum abundance. During 3 years of observation (summers of 2009, 2010, and 2011), we observed M. rubrum cells bearing numerous cryptophytes attached to the cirri throughout the estuary, especially during the bloom initiation phase and particularly in the peripheral bays. We performed a laboratory investigation in 2011 in which cryptophyte prey were introduced to high-density red-water samples in aquarium tanks. Within 2 h, individual M. rubrum cells collected multiple cryptophytes on their cirri, likely as a precursor to ingestion. The cells ceased their jumping motion and instead exhibited an undulation of the cirri and drifted slowly. We hypothesize that the availability and type of cryptophyte prey is important for bloom formation and that the acquisition of several cryptophytes at once by M. rubrum may be indicative of its ability to 'gather' or concentrate cryptophytes from the environment.KEY WORDS: Aquatic protists · Mesodinium rubrum · Teleaulax amphioxeia · Columbia River estuary · Ciliate · Cryptophyte · Predator-prey Resale or republication not permitted without written consent of the publisherAquat Microb Ecol 68: [117][118][119][120][121][122][123][124][125][126][127][128][129][130] 2013 late gene expression in plastids from multiple cryptophyte prey within the cell. The expression of nuclearencoded plastid genes declined as the number of sequestered nuclei disappeared from the population, suggesting that periodic consumption of prey is required by the ciliate to maintain chloroplast function (Johnson et al. 2007). Plastid sequestration is commonly observed in ciliates (Stoecker et al. 1988) and has recently been confirmed in the dinoflagellate Dinophysis caudata (Minnhagen et al. 2011).In contrast, Danish isolates of Mesodinium rubrum maintained the same number of chloroplasts over several divisions in culture, leading to reject the karyoklepty hypothesis in favor of the presence of a permanent endosymbiont. Since it has been clearly demonstrated that they are capable of -and that at least some isolates appear to require -feeding to sustain rapid growth, it has been suggested that M. rubrum depends on periodic ingestion of cryptophyte algae to sustain high growth rates (Johnson 2011). Thus far, both Korean (Park et al. 2007) and Danish ) M. rubrum isolates have exhibited a preference for cryptophytes of the Teleaulax / Plagioselmis / Geminigera clade to sustain maximal growth rates. These data indicate that the availability of appro...

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Extrusomes in Ciliates: Diversification, Distribution, and Phylogenetic Implications

Cited by 99 publications

References 137 publications

Independent Transport and Sorting of Functionally Distinct Protein Families in Tetrahymena thermophila Dense Core Secretory Granules

Independent Transport and Sorting of Functionally Distinct Protein Families in Tetrahymena thermophila Dense Core Secretory Granules

Morphologic and molecular description of Metopus fuscus Kahl from North America and new rDNA sequences from seven metopids (Armophorea, Metopidae)

Associations between Mesodinium rubrum and cryptophyte algae in the Columbia River estuary

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