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Sexual reproduction of Entomoneis cf. paludosa (Bacillariophyta)
Abstract
Sexual reproduction and the life cycle of the marine pennate diatom Entomoneis cf. paludosa are described. The reproduction in this species is characterized by morphological and behavioral isogamy. Two gametangia are involved in the sexual process, each of which produces two gametes.
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Experiments with clonal cultures of four pennate diatoms Haslea karadagensis, H. ostrearia, Pleurosigma sp. and Pseudo-nitzschia cf. seriata revealed that adding of sodium thiosulfate to the culture medium resulted in increase of algae growth rate. The highest, approximately two-fold, increase of the growth rate was observed in Pseudo-nitzschia cf. seriata, a member of the genus including toxicogenous species. Dependence of the algae growth rate on concentration of sodium thiosulfate was studied; optimal concentrations providing the highest growth rate were determined. Addition of ferrous-ammonium citrate or replacement of ferric chloride with ferrous-ammonium citrate did not affect the growth rate of the diatoms studied. For practical reasons, it is useful to prepare culture medium with the salinity of 36 ‰. Modified recipe of the ESAW medium is given.
The diatom genus Entomoneis includes species with aunique morphology,having panduriform frustules in girdle view,o ften twisted about its apical axis, with some unique characters such as as igmoid raphe on elevated bilobate keel, differently shaped junction lines, numerous girdle bands and variously perforated striae. Most of the species belonging to this genus are found to be brackish or marine, with some occurrences in freshwater habitats, but not one species has been described as exclusively freshwater.I nt his study,t he new freshwater diatom species Entomoneis triundulata sp. nov.i sd escribed based on a detailed morphological observation using light and scanning electron microscopy.T he specificfeaturesofE. triundulata are its triundulate valve margin; the shape of the transition between keel and valve body having ap roximal U-shaped end, as lightly curved middle segment and adistal V-shaped end; and five sub-compartments to the frustule cavity.Besides morphological features unique to E. triundulata,s imilarities with other Entomoneis species are reported and discussed. Keel /n ew species /r educed striae /r everse S-shape /S urirellales
The molecular evolutionary genetics analysis (Mega) software implements many analytical methods and tools for phylogenomics and phylomedicine. Here, we report a transformation of Mega to enable cross-platform use on Microsoft Windows and Linux operating systems. Mega X does not require virtualization or emulation software and provides a uniform user experience across platforms. Mega X has additionally been upgraded to use multiple computing cores for many molecular evolutionary analyses. Mega X is available in two interfaces (graphical and command line) and can be downloaded from www.megasoftware.net free of charge.
The genus Entomoneis Ehrenberg includes diatoms with structurally complex frustules having a bilobate keel elevated above the valve surface and numerous girdle bands. We describe here a new member of the genus, Entomoneis tenera sp. nov., a minute species found in the plankton of the south-eastern Adriatic Sea. The description and proposed taxonomic affiliation are based on both morphological observations and molecular analyses obtained from three cultivated strains. The cultures were established from plankton net samples taken during BIOTA (Bio-tracing Adriatic Water Masses) cruise conducted in February–March 2015. In addition to characteristic Entomoneis features such as panduriform cells, often twisted around the apical axis and a raphe with simple endings positioned on the sigmoid keel, morphological characteristics of E. tenera are: (1) very small cells, 16–21 μm long and 5–20 μm wide (2) very lightly silicified, delicate frustules without valve striation discernible in light microscopy, (3) broad lanceolate valves with scalpeliform apices (4) a straight to slightly arcuate junction line. Phylogenetic analyses using SSU, rbcL and psbC supported the position of E. tenera within the Entomoneis genus with a clear separation from the other described species.
The current study aims to enhance the understanding of the distribution and morphology of the diatom Entomoneis paludosa W Smith 1853 in African waters. The type material of Entomoneis paludosa (W Smith) Reimer was examined using light and scanning electron microscopy and the morphological characters were compared with new specimens sampled from a temperate river in South Africa. The wider distribution of this taxon on the African continent is discussed, and its relationship to water quality variables.
A new fossil diatom with a well-developed raphe-bearing keel and continuous junction line in the strongly bilobate wings is described as Entomoneis calixasini Paillès, Blanc-Valleron & Poulin sp. nov. This species was found at numerous levels within a 4.6-m-long core recovered from the north-western slope of the Central High of the Marmara Sea, Turkey. Detailed light and scanning electron microscopy were used to characterize this species. Entomoneis calixasini is unique by a wing resembling interconnecting dunces' caps. This species, sometimes the most abundant, is present between 44 and 395 cm of MET09-GR02 core sediments, corresponding to the Pleistocene last glacial period (brackish lacustrine sediments). It was not observed in the marine sediments above, or in other core sediments from the Marmara Sea or elsewhere in Pleistocene or Holocene sequences. It is absent in modern collections and from the literature, and is considered extinct.
Abstract: Amphora Ehrenb. ex Kütz. is a large heterogeneous genus, which lacks an adequate diagnosis and requires revision. Protoplast structure, plastid division and sexual reproduction are described for Amphora arcus Greg. and used as a basis for a discussion of relationships within the genus. An apparently natural group can be distinguished within Amphora sensu lato, characterized by the presence of a single ventral plastid, rearrangement of the gametes within both gametangia before plasmogamy, morphological and physiological isogamy, and expansion of the auxospores at right angles to the apical axes of the gametangia. The species belonging to this group are drawn from five of the nine subgenera recognized in the classic account of Amphora by Cleve and include the type species, A. ovalis (Kütz.) Kütz., as well as A. arcus. Some other Amphora species are not closely related to A. ovalis and A. arcus, and will need to be removed into new or resurrected genera. Cleve's subgenera are not themselves an adequate basis for revision, since most of them are heterogeneous. A lectotype is designated for A. arcus
Sexual reproduction and mating system of the freshwater diatom Ulnaria ulna (Nitzsch) Compère were studied by using clonal cultures. Mating system of the species involves homo-and heterothallic modes of reproduction; and both male and female clones were capable of homothallic reproduction. Two types of gametogenesis corresponding to two mating types were investigated. Analysis of the crossing table, gamete morphology, and sex distribution in the progeny resulted from intraclonal reproduction provided evidences that anisogamy and two mating types were determined in U. ulna genetically; male and female clones were hetero-and homogametic correspondently. Specific active movement of male gametes caused by the formation and retraction of pseudopodia-like structures on the gam-ete surface was described. The absence of reproductive isolation between clones gathered from geographically distant populations suggests continuity and broad distribution of the species. K e y w o r d s : Ulnaria ulna, mating system, sexual reproduction, gametogenesis, gametes movement, reproductive isolation. Introduction Last three decades brought us numerous publications, which indicated hetero-thallic character of mating system in many pennate diatoms and others). Biparental sex distribution suggests clear strategy of breeding experiments in pair combination of clones. Surprisingly, in the be-ginning experiments with Ulnaria ulna we received unexpected results. Signs of auxosporulation, i.e. gametes, empty gametangial frustules, zygotes, young and growing auxospores, etc. were found almost in all pair cross combina-tions. However, careful investigation of the pattern of sexual reproduction allowed us revealing two types of gametogenesis and corresponding modes of gametes behaviour that elucidated mating system and mysterious "panmixia" of clones in this species. The strategy of fertilization in araphid sessile diatoms is fairly diverse. In some araphid species parental cells need to be lain down
Chloroplast, mating behaviour, and auxosporulation are described for Amphora cf. proteus Gregory. The interphase chloroplast is butterfly-shaped and lies with its central part, containing a flat discoid pyrenoid, pressed against the ventral side of the girdle. Chloroplast division is longitudinal and begins and ends before mitosis and cytokinesis. Over the cell cycle, no rotations or lateral translocations of the chloroplast were noticed. A. cf. profeus is the first species of this genus in which sexual reproduction and breeding behaviour have been studied in clonal cultures. The cells isolated exhibited strictly dioecious behaviour, reproducing only in mixed cultures of sexually compatible clones. Sexual reproduction in A cf. proteus is morphologically and behaviourally isogamous. Each gametangium forms two functional gametes, which do not rearrange within the gametangium, and two small aborted cells. The aborted cells are produced after an unequal cytokinesis accompanying meiosis II; the second cytokinesis during gametogenesis represents a phenomenon hitherto unknown in pennate diatoms. Auxospore development takes place by bipolar expansion. The expansion is unequal on the two long sides of the auxospore, so that the auxospore becomes curved and dorsiventral. The auxospore forms a transverse and longitudinal perizonium.
Monoecious, bisexual and unisexual clones of Achnanthes longipes were isolated from the Black Sea and studied in laboratory culture. Clones differed in their growth characteristics : in monoecious clones the cells formed tufted aggregations while in other clones they were more dispersed. Bisexual and unisexual clones exhibited intraclonal (monoecious) reproduction, but only at a very low frequency and usually within a more restricted size range than in monoecious clones. Interclonal crosses were made in all possible pairwise combinations. Abundant auxosporulation took place in all crosses, except where unisexual clones of the same sex were incubated together. Auxosporulation was more vigorous and occurred over a wider size range in interclonal crosses than during monoecious reproduction. Sexual reproduction is isogamous. In the commonest pattern of auxosporulation, two paired gametangia each produce two gametes, which fuse to give two auxospores. More rarely (9% of pairs), the gametangia produce only one gamete apiece, and hence only one auxospore. In addition, very small cells can enlarge vegetatively, although genetic or cytological damage sometimes compromises their long-term viability.
Sexual reproduction in N. protracta is isogamous, although one gametangium often dehisces, releasing its gametes, before the other gametangium has completed meiosis. Sexualized cells produce an envelope of mucilage, into which the gametes are released and within which the zygotes begin their development. Two gametes are produced per gametangium and the supernumerary nuclei begin to degenerate very quickly after meiosis II. The young auxospores lie between the empty gametangia and are ellipsoidal. Expansion of the auxospores takes place in directions bearing no fixed relation to the orientation of the gametangia. The initial epivalve lacks pseudosepta, while the rostrate poles of the vegetative cells must develop during size reduction, being absent from the initial cell. Comparisons with Navicula sensu stricto show no significant similarities in sexual reproduction or frustule structure. Thus, in spite of their superficially similar protoplast structure, N. protracta is probably not closely related to Navicula sensu stricto; instead its affinities seem to lie with Parlibellus.
Clones of the domoic-acid-producing pennate diatom Pseudo-nitzschia multiseries (Hasle) Hasle and of the potentially toxic P. pseudodelicatissima (Hasle) Hasle normally decrease in cell size in culture until they eventually die without undergoing sexual reproduction to regain the largest cell size. However, we induced sexual reproduction by mixing individual exponentially growing clonal cultures of the appropriate minimal cell size under the same conditions that are normal for vegetative growth. We observed pairing of parent cells (gametangiogamy); production of four morphologically isogamous, nonflagellated gametes per gametangial pair; rearrangement of the gametes and their fusion to form zygotes, revealing physiological anisogamy; enlargement of auxospores; and formation of long initial cells. Our observations of allogamous reproduction are consistent with those reported for other dioecious pennate diatoms. Clones of P. pseudodelicatissima from the Black Sea and from the CCMP culture collection failed to auxosporulate when mixed together, although they are the same species according to scanning electron microscopy. The range in apical length of P. multiseries was broader than that reported in the literature for field samples, necessitating a modification of the species description. Knowledge of the pattern and timing of sexual reproduction in Pseudo-nitzschia spp. may provide insights into their bloom dynamics.
Arctic marine unicellular eukaryotes are composed of microalgae and non-autotrophic protists. These eukaryotes comprise a
well-diversified group of organisms that are either adapted to live in the upper water column of coastal and oceanic regions,
here defined as phytoplankton/pelagic communities, or in bottom horizons of sea ice and known as sympagic/sea-ice-associated
communities. There are approximately 5,000 recognized legitimate marine phytoplankton species and an unknown number of sympagic
eukaryotes. Although pelagic and sea-ice eukaryotes have been described since the exploration phase of the Arctic regions
up to the early twentieth century, no synthesis regarding information from all Arctic seas have been undertaken, and no exhaustive
current information provides the exact number and composition of species on a pan-Arctic scale. In a first attempt to assess
the pan-Arctic diversity of pelagic and sea-ice eukaryotes, a wealth of data from various sources (e.g., scientific publications,
unpublished reports, databases) were reviewed, while taxonomic data were confirmed with current nomenclature and classification.
We report a total of 2,106 marine single-celled eukaryote taxa with 1,874 phytoplankton and 1,027 sympagic taxa from four
grouped pan-Arctic regions, namely Alaska, Canada, Scandinavia including Greenland and the Russian Federation. Both phytoplankton
and sympagic taxa were present in four of the six super-groups of eukaryotes described by Adl et al. (J Eukaryot Microbiol
52:399-451, 2005), which are Archaeplastida (chlorophytes and prasinophytes), Chromalveolata (e.g., chrysophytes, cryptophytes, diatoms, dictyochophytes,
dinoflagellates and prymnesiophytes), Excavata (euglenids) and Opisthokonta (choanoflagellates). The bulk of this marine biodiversity
of Arctic microorganisms consists of large cells (>20μm) mainly due to examination at low magnification under light microscopy.
Future efforts should focus enhancing our knowledge of the biological diversity of small cells (<20μm), which represent less
than 20% of our actual biodiversity assessment of pan-Arctic regions.
KeywordsArctic–Biodiversity–Pelagic–Sea ice–Unicellular eukaryotes
Zinc-supplementation (20 μM) effects on growth, photosynthesis, antioxidant enzyme activities (superoxide dismutase, ascorbate peroxidase, catalase), and the expression of phytochelatin synthase gene were investigated in four marine diatoms (Amphora acutiuscula, Nitzschia palea, Amphora coffeaeformis and Entomoneis paludosa). Zn-supplementation reduced the maximum cell density. A linear relationship was found between the evolution of gross photosynthesis and total chlorophyll content. The Zn treatment decreased the electron transport rate except in A. coffeaeformis and in E. paludosa at high irradiance. A linear relationship was found between the efficiency of light to evolve oxygen and the size of the light-harvesting antenna. The external carbonic anhydrase activity was stimulated in Zn-supplemented E. paludosa but was not correlated with an increase of photosynthesis. The total activity of the antioxidant enzymes did not display any clear increase except in ascorbate peroxidase activity in N. palea. The phytochelatin synthase gene was identified in the four diatoms, but its expression was only revealed in N. palea, without a clear difference between control and Zn-supplemented cells. Among the four species, A. paludosa was the most sensitive and A. coffeaeformis, the most tolerant. A. acutiuscula seemed to be under metal starvation, whereas, to survive, only N. palea developed several stress responses.
During sexual reproduction, araphid pennate diatoms of the genus Tabularia (Kützing) D. M. Williams and Round released male gametes directly into the medium, sometimes at a considerable distance from the female gametes. This raised the question of how male gametes, suspended in water, manage to reach female ones, given that no locomotive organelles have been described in gametes of pennate diatoms. Optical microscopic investigation revealed cytoplasmic projections produced by male gametes of Tabularia tabulata (C. A. Agardh) Snoeijs and T. fasciculata (C. A. Agardh) D. M. Williams and Round. Morphology and behavior of these projections is consistent with pseudopodia, however, which specific type of pseudopodia they may be, remains inconclusive. The growth and retraction of the pseudopodia coincided with gamete motility and so we postulate that it explains the otherwise apparent random movement of male gametes. Spinning, shuffling and chaotic patterns of motility were documented. In theory, gamete mobility increases the probability of gamete encounter thus enhancing the probability of syngamy. This is the first known case where cytoplasmic projections have been described in diatom gametes, and possibly in mature gametes in general.
Background:
Diatoms belong to the stramenopiles, one of the largest groups of eukaryotes, which are primarily characterized by a presence of an anterior flagellum with tubular mastigonemes and usually a second, smooth flagellum. Based on cell wall morphology, diatoms have historically been divided into centrics and pennates, of which only the former have flagella and only on the sperm. Molecular phylogenies show the pennates to have evolved from among the centrics. However, the timing of flagellum loss--whether before the evolution of the pennate lineage or after--is unknown, because sexual reproduction has been so little studied in the 'araphid' basal pennate lineages, to which Pseudostaurosira belongs.
Methods/principal finding:
Sexual reproduction of an araphid pennate, Pseudostaurosira trainorii, was studied with light microscopy (including time lapse observations and immunofluorescence staining observed under confocal scanning laser microscopy) and SEM. We show that the species produces motile male gametes. Motility is mostly associated with the extrusion and retrieval of microtubule-based 'threads', which are structures hitherto unknown in stramenopiles, their number varying from one to three per cell. We also report experimental evidence for sex pheromones that reciprocally stimulate sexualization of compatible clones and orientate motility of the male gametes after an initial 'random walk'.
Conclusions/significance:
The threads superficially resemble flagella, in that both are produced by male gametes and contain microtubules. However, one striking difference is that threads cannot beat or undulate and have no motility of their own, and they do not bear mastigonemes. Threads are sticky and catch and draw objects, including eggs. The motility conferred by the threads is probably crucial for sexual reproduction of P. trainorii, because this diatom is non-motile in its vegetative stage but obligately outbreeding. Our pheromone experiments are the first studies in which gametogenesis has been induced in diatoms by cell-free exudates, opening new possibilities for molecular 'dissection' of sexualization.
Diatom species composition in the ice of Velikaya Salma strait of Kandalaksha Bay of the White Sea was studied in 5 stations in March, 2013–2014—prior to the spring algal bloom. Under-ice water salinity and ice thickness did not differ significantly between the two years. In total 59 diatom taxa (47 species and 12 taxa of higher taxonomic ranks) were found in the ice of Velikaya Salma strait, which makes 61% of the number of diatom taxa found in Velikaya Salma ice during the whole ice period and 22% of all the White Sea ice species. Species Stenoneis obtuserostrata (Hustedt) Poulin and Gyrosigma concilians (Cleve) Okolodkov were identified in the White Sea ice for the first time. Szymkiewicz-Simpson similarity coefficient for pairs of stations with significant difference was 0.44–0.80.
The focus of this paper is the sexual reproduction and phylogeny of Schizostauron Grunow, which were studied using clonal cultures isolated from the Indian Ocean coast of Mozambique near Tofo and Bazaruto. Taxa of Schizostauron were characterized by light and electron microscopy and a phylogeny derived from three genes (rbcL, psbC and short subunit). Schizostauron was established in the second half of the 19th century, then forgotten, with its taxa included in Cocconeis or Achnanthes sensu lato. Schizostauron, together with Astartiella and perhaps also Kolbesia and Karayevia, seems to form a third lineage of monoraphid diatoms, which are related to biraphid diatoms belonging to the Stauroneidaceae and Parlibellus, but not to the two other lineages of monoraphids (Achnanthes and the Achnanthidiaceae-Cocconeidaceae group). In culture, size reduction was followed by release of gametes and auxosporulation in mixtures of clones. Despite some morphological differences, four clones from the Bazaruto population proved to be sexually compatible, one of the clones being sexually compatible with the three others. Before gametogenesis, cells gathered in groups of two to eight through active movement. Some groups of cells surrounded themselves by weakly visible mucilage. Reproduction was isogamous morphologically, and apparently also behaviourally. Growing auxospores were surrounded by the empty irregularly arranged frustules of parental cells. In numerous aspects the pattern of sexual reproduction of Schizostauron is similar to that of Achnanthes sensu stricto. The rbcL identity matrix (IDM) for sexually compatible clones ranged between 0.998 and 0.984. One clone derived from the Tofo population had an IDM below 0.900 and was sexually isolated from the remaining clones. A description of Schizostauron davidovichiorum sp. Nov. is provided.
Sexual auxosporulation was observed in a mixed culture of two strains of Navicula directa var. directa. Two gametes did not re-arrange in their gametangium and each adhered to the inner surfaces of the gametangial theca. Each of the two gametes of one gametangium fused with a gamete of the other gametangium iso-gamously. As a result, two zygotes and hence two auxo-spores were produced per paired gametangia. As the gametangial thecae kept close to the gametes during fusion, the zygote became associated with two different thecae. The presence of type IB2a of Geitler's (1973) system was confirmed by the present observations.
A hyaline Entomoneis species was isolated during a study of microbial mats from hypersaline environments in the Exportadora de Sal salt works, Guerrero Negro (Mexico). Morphological, ultrastructural and ecophysiological characteristics of the species were investigated. Live cells contained two plastids. In girdle view the frustules appeared bilobate, deeply constricted, with a junction line visible only near the central nodule. The margin of the wings was fibulate with 19–23 fibulae in 10 urn, some of which, at irregular intervals, appeared longer and ended in small puncta. After mild cleaning, neither valve body nor the sigmoid connecting bands appeared ornamented under the light microscope. Scanning electron microscopy revealed membranaceous valves without ornamentation and a strongly silicified fibulate keel. Furthermore, keels were the only part of the cell which could be found and recognized in cleaned field samples. This diatom species was able to grow over a salinity range of 15–50 ‰ and hence could be considered a euryhaline marine species.
Auxospore formation in Nitzschia recta and N. sigmoidea is associated with allogamous sexual reproduction, in which two vegetative cells pair and function as gametangia. Each gametangium produces two morphologically identical gametes, one of which is active and the other passive (trans-behavioural anisogamy). The gametes become re-arranged within the gametangia and then the active gametes migrate through a narrow copulation tube to effect plasmogamy. The copulation tube has an organic wall and is produced by fusion of two papillae, whch grow out through localized splits in the gametangial frustules during meiotic prophase. The auxospores do not have an obvious perizonium and expand parallel to the apical axes of the gametangia. The same kind of reproduction occurs in N. dissipata and N. flexoides, supporting the idea that all these species form a natural group, also characterized by the presence of conopea on the valves. Reproductive and other characters suggest that Nitzschia and its allies may have evolved from an amphoroid ancestor.
Twelve clonal cultures of the marine pennate diatom Haslea ostrearia (Gaillon) Simonsen were used to study sexual reproduction and auxosporulation. After crossing, compatible gametangia paired girdle to girdle, with no visible surrounding mucilage. Two gametes were formed per gametangium; these were not attached to the thecae of the parental frustule and gametes from one gametangium fused with the gametes from the other gametangium. Sexual reproduction was isogamous, resulting in the production of two zygotes per paired gametangia. The pattern of reproduction in H. ostrearia can be classified as type IB2a according to Geitler's system. The expansion of auxospores, which was bipolar, was accompanied by the formation of a transverse perizonium. Superfluous nuclei resulting from meiosis were not visible. The upper limit of the cell size range suitable for sexualization was c. 68 µm, i.e. about half the maximum species-specific size of about 140 µm. Sexual reproduction has been shown by previous authors to occur in clonal cultures and our observations confirm that two modes of sexual reproduction, homothallic and heterothallic, coexist in H. ostrearia.
The cytology and life cycle of Pinnularia cf. gibba was examined in nine clones from three Scottish localities. This freshwater epipelic diatom is heterothallic and produces two isogametes per gametangium in type IC auxosporulation (Geitler's classification [1973]). The zygote undergoes a highly unusual metamorphosis before beginning expansion, becoming shortly linear–lanceolate; this is accompanied by formation of a complete covering of thin, oxidation-resistant strips and scale-like structures (at the poles), which are quite separate from the perizonium formed during auxospore expansion. Observations of similar incunabular structures in P. acidojaponica show that these elements are siliceous. The P. cf. gibba perizonium also has unusual features, including a remarkably wide primary band. Trikaryotic and haploid auxospores are sometimes formed and haploid ‘zygotes’ mature and expand like diploids, but do not develop into mature initial cells. Several phases of mucilage secretion take place, from the gametangia, zygotes and auxospores. Triplets of gametangia and polyspermy occurred with high frequency; this and the systematic significance of variation in auxospore, incunabula and perizonium structure, are discussed. Aspects of the taxonomy of the P. gibba group are treated in supplementary material provided on the European Journal of Phycology website.
Sexual reproduction takes many forms within the diatoms. The variation has been classified by several authors, but in most cases the distinctions between their main categories have depended on the number of gametes produced per gametangium (and thus on how many zygotes per pair of copulating cells), and upon whether fusion is oogamous, anisogamous or isogamous. These classifications are not themselves an adequate basis for taxonomic comparison, which should be based on individual characteristics of the sexual process. Diatoms seem to be primitively oogamous. In araphid pennate diatoms and some raphid diatoms the gametes and gametangia are morphologically alike but physiologically distinct; one gametangium produces active gametes and the other passive ones. This may be the primitive condition in pennate diatoms, providing a link to the oogamy of centrics via the morphological anisogamy of Rhabdonema Ktz.
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