Pub Date : 2021-10-12DOI: 10.1080/09670262.2021.1966838
L. Arin, Albert Reñé, R. Gallisai, D. Sarno, E. Garcés, M. Estrada
ABSTRACT The majority of species of the highly diverse genus Chaetoceros are described as chain-forming, although several species are described as strictly solitary (such as C. tenuissimus) or having an alternate solitary and a chain-forming phase during their life history (such as C. salsugineus). In this study, the diversity of small forms of Chaetoceros from the NW Mediterranean coastal waters was explored through the morphological and molecular characterization of four different strains belonging to two distinct species. Based on their morphology, three of the strains were identified as C. salsugineus (Takano, 1983). The SSU and LSU rDNA sequences represented the first available for well-characterized C. salsugineus strains and were 96.6–100% similar to publicly available C. tenuissimus (Meunier, 1913) sequences. Both species share the same morphological features, such as setae and ultrastructure of the valves, as well as the rimoportula characteristics. In addition, the morphology of the solitary form of C. salsugineus matched with that of C. tenuissimus. Here, we propose the two species as synonyms (the name C. tenuissimus prevailing as it has priority for this taxon), emend the original description and designate an epitype. The fourth strain was identified as C. olympicus sp. nov., a new species, which alternates solitary and chain-forming forms within its life history. The main differential characteristics of this species are the absence of rimoportula both in terminal and intercalary valves, the setae ultrastructure, which is thin and circular in cross-section with a few, slightly twisted, rows of small rectangular poroids and some spirally arranged spines, and the morphology of the resting spores, with primary valve vaulted and covered with short to medium-sized spines, and secondary valve smaller, rounded and smooth. A comparison of C. tenuissimus and C. olympicus with other species as well as information on their life cycle and ecology is also provided. HIGHLIGHTS • Description of a new Chaetoceros species: C. olympicus. • Proposal that C. tenuissimus and C. salsugineus are synonyms. • Importance of morphological variability in life cycles for species identification.
{"title":"Taxonomic relationship between two small-sized Chaetoceros species (Bacillariophyta): C. tenuissimus and C. salsugineus, and comparison with C. olympicus sp. nov. from Catalan coastal waters (NW Mediterranean)","authors":"L. Arin, Albert Reñé, R. Gallisai, D. Sarno, E. Garcés, M. Estrada","doi":"10.1080/09670262.2021.1966838","DOIUrl":"https://doi.org/10.1080/09670262.2021.1966838","url":null,"abstract":"ABSTRACT The majority of species of the highly diverse genus Chaetoceros are described as chain-forming, although several species are described as strictly solitary (such as C. tenuissimus) or having an alternate solitary and a chain-forming phase during their life history (such as C. salsugineus). In this study, the diversity of small forms of Chaetoceros from the NW Mediterranean coastal waters was explored through the morphological and molecular characterization of four different strains belonging to two distinct species. Based on their morphology, three of the strains were identified as C. salsugineus (Takano, 1983). The SSU and LSU rDNA sequences represented the first available for well-characterized C. salsugineus strains and were 96.6–100% similar to publicly available C. tenuissimus (Meunier, 1913) sequences. Both species share the same morphological features, such as setae and ultrastructure of the valves, as well as the rimoportula characteristics. In addition, the morphology of the solitary form of C. salsugineus matched with that of C. tenuissimus. Here, we propose the two species as synonyms (the name C. tenuissimus prevailing as it has priority for this taxon), emend the original description and designate an epitype. The fourth strain was identified as C. olympicus sp. nov., a new species, which alternates solitary and chain-forming forms within its life history. The main differential characteristics of this species are the absence of rimoportula both in terminal and intercalary valves, the setae ultrastructure, which is thin and circular in cross-section with a few, slightly twisted, rows of small rectangular poroids and some spirally arranged spines, and the morphology of the resting spores, with primary valve vaulted and covered with short to medium-sized spines, and secondary valve smaller, rounded and smooth. A comparison of C. tenuissimus and C. olympicus with other species as well as information on their life cycle and ecology is also provided. HIGHLIGHTS • Description of a new Chaetoceros species: C. olympicus. • Proposal that C. tenuissimus and C. salsugineus are synonyms. • Importance of morphological variability in life cycles for species identification.","PeriodicalId":12032,"journal":{"name":"European Journal of Phycology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2021-10-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"49635437","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2021-10-04DOI: 10.1080/09670262.2021.1950839
Luana Miranda Coutinho, Fernanda Penelas Gomes, M. Nasri Sissini, Talita Vieira-Pinto, Maria Carolina Muller de Oliveira Henriques, M. C. Oliveira, Paulo Antunes Horta, Maria Beatriz Barbosa de Barros Barreto
ABSTRACT Molecular studies have revealed cryptic diversity and polyphyly in the genus Lithothamnion. In this study we aimed to investigate the diversity and phylogeny of specimens that are morphologically described as Lithothamnion based on extensive collections along the Brazilian coast and an integrative taxonomic approach. Our results led to the proposal of Roseolithon gen. nov. belonging to the subfamily Melobesioideae. This new genus is described from the tropical north-western Atlantic and warm temperate south-western Atlantic specimens, based on phylogenetic analyses of psbA, rbcL-3P, COI-5P and SSU rDNA molecular markers, species delimitation methods, genetic divergence and morpho-anatomical observations. The integrative approach led us to find a set of morphological features that characterize Roseolithon: (i) thallus organization monomerous with plumose hypothallus (non-coaxial); (ii) flared epithallial cells; (iii) subepithallial cells varying in size and may be shorter, approximately equal to or longer than those subtending them; (iv) cells of adjacent filaments linked by fusions; (v) tetra/bisporangial conceptacle chambers multiporate; and (vi) the presence of pore canals bordered by rosette cells in depressions giving the surface a pitted appearance. Depending on the species, this pitted appearance occurs due to the sunken or disintegrated rosette cell roofs. The grade of the degeneration of the rosette cell roofs characterizes the species of this genus. The new genus Roseolithon is composed of at least 18 species, of which we describe seven new species: Roseolithon tupii, R. tamoioi, R. tremembei, R. potiguarae, R. karaiborum, R. purii and R. goytacae. Highlights Phylogenetic analyses revealed Lithothamnion to be a polyFphyletic genus. Integrative taxonomy enabled the description of a new genus Roseolithon. Morpho-anatomy does not reflect molecular phylogeny of non-geniculate coralline algae.
{"title":"Cryptic diversity in non-geniculate coralline algae: a new genus Roseolithon (Hapalidiales, Rhodophyta) and seven new species from the Western Atlantic","authors":"Luana Miranda Coutinho, Fernanda Penelas Gomes, M. Nasri Sissini, Talita Vieira-Pinto, Maria Carolina Muller de Oliveira Henriques, M. C. Oliveira, Paulo Antunes Horta, Maria Beatriz Barbosa de Barros Barreto","doi":"10.1080/09670262.2021.1950839","DOIUrl":"https://doi.org/10.1080/09670262.2021.1950839","url":null,"abstract":"ABSTRACT Molecular studies have revealed cryptic diversity and polyphyly in the genus Lithothamnion. In this study we aimed to investigate the diversity and phylogeny of specimens that are morphologically described as Lithothamnion based on extensive collections along the Brazilian coast and an integrative taxonomic approach. Our results led to the proposal of Roseolithon gen. nov. belonging to the subfamily Melobesioideae. This new genus is described from the tropical north-western Atlantic and warm temperate south-western Atlantic specimens, based on phylogenetic analyses of psbA, rbcL-3P, COI-5P and SSU rDNA molecular markers, species delimitation methods, genetic divergence and morpho-anatomical observations. The integrative approach led us to find a set of morphological features that characterize Roseolithon: (i) thallus organization monomerous with plumose hypothallus (non-coaxial); (ii) flared epithallial cells; (iii) subepithallial cells varying in size and may be shorter, approximately equal to or longer than those subtending them; (iv) cells of adjacent filaments linked by fusions; (v) tetra/bisporangial conceptacle chambers multiporate; and (vi) the presence of pore canals bordered by rosette cells in depressions giving the surface a pitted appearance. Depending on the species, this pitted appearance occurs due to the sunken or disintegrated rosette cell roofs. The grade of the degeneration of the rosette cell roofs characterizes the species of this genus. The new genus Roseolithon is composed of at least 18 species, of which we describe seven new species: Roseolithon tupii, R. tamoioi, R. tremembei, R. potiguarae, R. karaiborum, R. purii and R. goytacae. Highlights Phylogenetic analyses revealed Lithothamnion to be a polyFphyletic genus. Integrative taxonomy enabled the description of a new genus Roseolithon. Morpho-anatomy does not reflect molecular phylogeny of non-geniculate coralline algae.","PeriodicalId":12032,"journal":{"name":"European Journal of Phycology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2021-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"59529206","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2021-09-28DOI: 10.1080/09670262.2021.1964608
Á. Cuadrado, M. Sixto, R. Figueroa, I. Bravo, A. de Bustos
ABSTRACT Dinoflagellates are protists with exceptionally large genomes and chromosomes that lack nucleosomes. To date, information on their genome organization is scarce. Studies investigating the distribution of ribosomal RNA genes (rDNA) in plants and animals by fluorescence in situ hybridization (FISH) have provided important information to elucidate the genome organization and evolution of many species. In the present study, FISH was used to analyse the chromosomal organization of 45S and 5S rDNA and the extent of rDNA variation among five species of Gambierdiscus (G. australes, G. excentricus, G. silvae, G. carolinianus and G. caribaeus). The results, the intensity and location of the FISH signals, are summarized as follows: (1) All Gambierdiscus species have extremely high copy number of 45S rDNA repeat units arranged in a large nucleolus situated in the concave region of the typical interphasic bean-shaped nucleus. In addition, outside the large nucleolus, G. silvae and G. carolinianus have minor clusters of 45S rDNA repeats. (2) Many copies of 5S rDNA organized in one or a few clusters, depending on the species, are physically separated from the 45S rDNA but located close, peripherally, to the nucleolus. This nuclear organization is preserved during cell division. (3) Gambierdiscus australes was the species with the lowest 5S rDNA FISH signals clustered into a single site. In contrast, one major and several minor 5S rDNA clusters of FISH signals were observed in G. excentricus. We find that the species analysed can be differentiated by their species-specific FISH rDNA phenotypes demonstrating the usefulness of FISH in comparative cytogenomic studies of Gambierdiscus. In addition, using G. australes as a model, we demonstrate the usefulness of 45S and 5S rDNA as chromosomal markers to study dinomitosis, the atypical nuclear division that solely occurs in the class Dinophyceae.
{"title":"Comparative FISH mapping of 45S and 5S rDNA in the genus Gambierdiscus advances understanding of the cytogenetic diversity and mitosis of dinoflagellates","authors":"Á. Cuadrado, M. Sixto, R. Figueroa, I. Bravo, A. de Bustos","doi":"10.1080/09670262.2021.1964608","DOIUrl":"https://doi.org/10.1080/09670262.2021.1964608","url":null,"abstract":"ABSTRACT Dinoflagellates are protists with exceptionally large genomes and chromosomes that lack nucleosomes. To date, information on their genome organization is scarce. Studies investigating the distribution of ribosomal RNA genes (rDNA) in plants and animals by fluorescence in situ hybridization (FISH) have provided important information to elucidate the genome organization and evolution of many species. In the present study, FISH was used to analyse the chromosomal organization of 45S and 5S rDNA and the extent of rDNA variation among five species of Gambierdiscus (G. australes, G. excentricus, G. silvae, G. carolinianus and G. caribaeus). The results, the intensity and location of the FISH signals, are summarized as follows: (1) All Gambierdiscus species have extremely high copy number of 45S rDNA repeat units arranged in a large nucleolus situated in the concave region of the typical interphasic bean-shaped nucleus. In addition, outside the large nucleolus, G. silvae and G. carolinianus have minor clusters of 45S rDNA repeats. (2) Many copies of 5S rDNA organized in one or a few clusters, depending on the species, are physically separated from the 45S rDNA but located close, peripherally, to the nucleolus. This nuclear organization is preserved during cell division. (3) Gambierdiscus australes was the species with the lowest 5S rDNA FISH signals clustered into a single site. In contrast, one major and several minor 5S rDNA clusters of FISH signals were observed in G. excentricus. We find that the species analysed can be differentiated by their species-specific FISH rDNA phenotypes demonstrating the usefulness of FISH in comparative cytogenomic studies of Gambierdiscus. In addition, using G. australes as a model, we demonstrate the usefulness of 45S and 5S rDNA as chromosomal markers to study dinomitosis, the atypical nuclear division that solely occurs in the class Dinophyceae.","PeriodicalId":12032,"journal":{"name":"European Journal of Phycology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2021-09-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"48793609","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2021-09-21DOI: 10.1080/09670262.2021.1970235
H. Kawai, T. Hanyuda, E. Henry
ABSTRACT Molecular phylogeny based on concatenated sequences of chloroplast atpB, psaA, psbA, psbC and rbcL genes indicates that the filamentous brown alga Pilinia rimosa is phylogenetically distant from the Ectocarpales, in which it has been classified (as Waerniella lucifuga). In the tree, Pilinia was sister to the clade comprised of Ishige and Petroderma (Ishigeales) supported by high statistical values. Observations of unialgal P. rimosa cultures originating from Helgoland (Germany), England (UK), Woods Hole (USA) and Newfoundland (Canada) showed a direct type of life history with reproduction by characteristic unilocular zoidangia typically forming only four zoids. Despite the description of plurilocular zoidangia in Kuckuck’s account as well as in later publications, we conclude that those observations were based on misinterpretation of the very small unilocular zoidangia formed in series, often with longitudinal walls between zoidangia. Pilinia rimosa grows in caves or crevices in rocks, and on walls or wood pilings in deep shade in the upper intertidal and spray zone, and is therefore regarded as a marine species, but it could also survive and mature in freshwater medium. We propose the establishment of a new family Piliniaceae for Pilinia and place it in Ishigeales. Molecular and morphological analysis of the culture strains, SAG 124.79 and SAG 2381, identified as the euryhaline alga Porterinema fluviatile, indicated that SAG 124.79 is in fact P. rimosa. However, SAG 2381 is true P. fluviatile, also displaying the characteristic plurilocular zoidangia. Porterinema was shown to be a member of the Chordariaceae, Ectocarpales sensu lato.
{"title":"Transfer of Pilinia from Ectocarpales to Ishigeales (Phaeophyceae) with proposal of Piliniaceae fam. nov., and taxonomy of Porterinema in Ectocarpales","authors":"H. Kawai, T. Hanyuda, E. Henry","doi":"10.1080/09670262.2021.1970235","DOIUrl":"https://doi.org/10.1080/09670262.2021.1970235","url":null,"abstract":"ABSTRACT Molecular phylogeny based on concatenated sequences of chloroplast atpB, psaA, psbA, psbC and rbcL genes indicates that the filamentous brown alga Pilinia rimosa is phylogenetically distant from the Ectocarpales, in which it has been classified (as Waerniella lucifuga). In the tree, Pilinia was sister to the clade comprised of Ishige and Petroderma (Ishigeales) supported by high statistical values. Observations of unialgal P. rimosa cultures originating from Helgoland (Germany), England (UK), Woods Hole (USA) and Newfoundland (Canada) showed a direct type of life history with reproduction by characteristic unilocular zoidangia typically forming only four zoids. Despite the description of plurilocular zoidangia in Kuckuck’s account as well as in later publications, we conclude that those observations were based on misinterpretation of the very small unilocular zoidangia formed in series, often with longitudinal walls between zoidangia. Pilinia rimosa grows in caves or crevices in rocks, and on walls or wood pilings in deep shade in the upper intertidal and spray zone, and is therefore regarded as a marine species, but it could also survive and mature in freshwater medium. We propose the establishment of a new family Piliniaceae for Pilinia and place it in Ishigeales. Molecular and morphological analysis of the culture strains, SAG 124.79 and SAG 2381, identified as the euryhaline alga Porterinema fluviatile, indicated that SAG 124.79 is in fact P. rimosa. However, SAG 2381 is true P. fluviatile, also displaying the characteristic plurilocular zoidangia. Porterinema was shown to be a member of the Chordariaceae, Ectocarpales sensu lato.","PeriodicalId":12032,"journal":{"name":"European Journal of Phycology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2021-09-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"47750352","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2021-09-07DOI: 10.1080/09670262.2021.1948614
U. Tillmann, A. Beran, M. Gottschling, Stephan Wietkamp, M. Hoppenrath
ABSTRACT The Prorocentrales are a unique group of dinophytes based on several apomorphic traits, but species delimitation is challenging within the group. Prorocentrum triestinum was described by Josef Schiller in 1918 as an important bloom-forming species from Trieste (Mediterranean, Adriatic Sea) with a conspicuous asymmetric outline and a small, asymmetrically located subapical spine. All subsequent records under this name fail to conform to Schiller’s original description. These inconsistencies have their origin in John Dodge’s 1975 revision of Prorocentrum, which placed Prorocentrum redfieldii, a more symmetrical, slender species with a long apical spine, into synonymy under P. triestinum. To clarify this confusion, we collected samples at the type locality of P. triestinum in Trieste and established a strain that is morphologically consistent with the protologue and suitable for use in epitypification. Morphology and rRNA sequence data of this strain were compared with four new strains identified as P. redfieldii from the Mediterranean Sea and the North Atlantic Ocean. Cells of P. triestinum had an asymmetric outline in lateral view and a small, dorso-subapical spine. These features, which are readily resolved by light microscopy, were distinct from those of the nearly symmetrical and slender cells of P. redfieldii, which had a long, apically located spine. The species are nevertheless closely related and share an identical architecture of the periflagellar area with a distinctive, largely reduced accessory pore together with a very small platelet 7. This apomorphy clearly differentiates both species from other species of Prorocentrum. Both species differ in their primary rRNA sequences, and ITS and LSU sequence differences will enable them to be distinguished in future meta-barcoding studies. The present study demonstrates that P. triestinum and P. redfieldii are distinct species and thus contributes to a reliable biodiversity assessment of Prorocentrum. HIGHLIGHTS Prorocentrum triestinum is characterised molecularly for the first time and delimited from P. redfieldii. The identity of important bloom-forming species is clarified. Structural details of the periflagellar area are described.
{"title":"Clarifying confusion – Prorocentrum triestinum J.Schiller and Prorocentrum redfieldii Bursa (Prorocentrales, Dinophyceae) are two different species","authors":"U. Tillmann, A. Beran, M. Gottschling, Stephan Wietkamp, M. Hoppenrath","doi":"10.1080/09670262.2021.1948614","DOIUrl":"https://doi.org/10.1080/09670262.2021.1948614","url":null,"abstract":"ABSTRACT The Prorocentrales are a unique group of dinophytes based on several apomorphic traits, but species delimitation is challenging within the group. Prorocentrum triestinum was described by Josef Schiller in 1918 as an important bloom-forming species from Trieste (Mediterranean, Adriatic Sea) with a conspicuous asymmetric outline and a small, asymmetrically located subapical spine. All subsequent records under this name fail to conform to Schiller’s original description. These inconsistencies have their origin in John Dodge’s 1975 revision of Prorocentrum, which placed Prorocentrum redfieldii, a more symmetrical, slender species with a long apical spine, into synonymy under P. triestinum. To clarify this confusion, we collected samples at the type locality of P. triestinum in Trieste and established a strain that is morphologically consistent with the protologue and suitable for use in epitypification. Morphology and rRNA sequence data of this strain were compared with four new strains identified as P. redfieldii from the Mediterranean Sea and the North Atlantic Ocean. Cells of P. triestinum had an asymmetric outline in lateral view and a small, dorso-subapical spine. These features, which are readily resolved by light microscopy, were distinct from those of the nearly symmetrical and slender cells of P. redfieldii, which had a long, apically located spine. The species are nevertheless closely related and share an identical architecture of the periflagellar area with a distinctive, largely reduced accessory pore together with a very small platelet 7. This apomorphy clearly differentiates both species from other species of Prorocentrum. Both species differ in their primary rRNA sequences, and ITS and LSU sequence differences will enable them to be distinguished in future meta-barcoding studies. The present study demonstrates that P. triestinum and P. redfieldii are distinct species and thus contributes to a reliable biodiversity assessment of Prorocentrum. HIGHLIGHTS Prorocentrum triestinum is characterised molecularly for the first time and delimited from P. redfieldii. The identity of important bloom-forming species is clarified. Structural details of the periflagellar area are described.","PeriodicalId":12032,"journal":{"name":"European Journal of Phycology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2021-09-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"43527139","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2021-09-06DOI: 10.1080/09670262.2021.1959653
H. Kawai, T. Hanyuda, Q. Cheng, K. Miller, A. Peters
ABSTRACT Dictyosiphon asiaticus sp. nov. and D. sparsus sp. nov. are newly described from Japan and the north-western Pacific. Molecular phylogenies based on the mitochondrial cox1 and cox3 and chloroplast atpB, psaA, psbA and rbcL DNA sequences revealed that Dictyosiphon comprises at least seven lineages worldwide. Japanese Dicytosiphon species formed two clades with high support and were sister to a clade including specimens from the cold-water regions of the northern Pacific, the Arctic, and the north-western Atlantic. Specimens of one of the Japanese clades (= D. asiaticus sp. nov.) were morphologically similar to D. foeniculaceus (generitype described from Scotland, UK), having densely branched thalli with fine branches, and were epiphytic on Scytosiphon spp. and Chordaria spp. Specimens of the other Japanese clade (= D. sparsus sp. nov.) were morphologically similar to D. chordaria, having somewhat thicker, sparse branches with blunt tips, and were epiphytic on Chordaria spp. We assign the third clade distributed on both sides of the North Pacific to D. sinicola, which was described from Washington, USA, for the following reasons: Dictyosiphon specimens in the region having relatively densely branched thalli with fine tips have been identified as D. foeniculaceus, and D. sinicola was distinguished from them by its remarkably larger thallus, while anatomically they are very similar. However, D. foeniculaceus is not widely distributed in the region, with only one genetic lineage (species) reported, so that those two taxa are considered to be ecotypes of the same species, and D. sinicola is the valid name for the taxon.
{"title":"Taxonomic revision of Dictyosiphon (Ectocarpales s.l., Phaeophyceae) from the north-western Pacific, with descriptions of D. asiaticus sp. nov. and D. sparsus sp. nov","authors":"H. Kawai, T. Hanyuda, Q. Cheng, K. Miller, A. Peters","doi":"10.1080/09670262.2021.1959653","DOIUrl":"https://doi.org/10.1080/09670262.2021.1959653","url":null,"abstract":"ABSTRACT Dictyosiphon asiaticus sp. nov. and D. sparsus sp. nov. are newly described from Japan and the north-western Pacific. Molecular phylogenies based on the mitochondrial cox1 and cox3 and chloroplast atpB, psaA, psbA and rbcL DNA sequences revealed that Dictyosiphon comprises at least seven lineages worldwide. Japanese Dicytosiphon species formed two clades with high support and were sister to a clade including specimens from the cold-water regions of the northern Pacific, the Arctic, and the north-western Atlantic. Specimens of one of the Japanese clades (= D. asiaticus sp. nov.) were morphologically similar to D. foeniculaceus (generitype described from Scotland, UK), having densely branched thalli with fine branches, and were epiphytic on Scytosiphon spp. and Chordaria spp. Specimens of the other Japanese clade (= D. sparsus sp. nov.) were morphologically similar to D. chordaria, having somewhat thicker, sparse branches with blunt tips, and were epiphytic on Chordaria spp. We assign the third clade distributed on both sides of the North Pacific to D. sinicola, which was described from Washington, USA, for the following reasons: Dictyosiphon specimens in the region having relatively densely branched thalli with fine tips have been identified as D. foeniculaceus, and D. sinicola was distinguished from them by its remarkably larger thallus, while anatomically they are very similar. However, D. foeniculaceus is not widely distributed in the region, with only one genetic lineage (species) reported, so that those two taxa are considered to be ecotypes of the same species, and D. sinicola is the valid name for the taxon.","PeriodicalId":12032,"journal":{"name":"European Journal of Phycology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2021-09-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"49647391","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2021-08-16DOI: 10.1080/09670262.2021.1923809
Benwen Liu, J. Ge, Huan Zhu, Shuyin Li, Xiaoqi Dong, Guoxiang Liu, Zhengyu Hu
ABSTRACT Chaetophora lobata is the type species of the polyphyletic genus Chaetophora. Clarification of its species identification, phylogenetic relationships, and plastome characteristics is helpful for taxonomic revisions and evolutionary studies of this genus. This study presents detailed information on morphology, culture, phylogenetic analysis, phylogenomics and comparative genomics of C. lobata. The complete morphological description and phylogenetic analyses based on nuclear rDNA and chloroplast protein-coding genes were robust for the identification of C. lobata. Moreover, de novo sequencing was used to determine the 222 213 bp chloroplast genome, which lacked inverted repeats as in all other members of the Chaetophorales. The chloroplast DNA (cpDNA) of C. lobata was found to be AT-rich (68.2%), consisting of 67 protein-coding genes, among which 62 genes were encoded on the plus strand and five genes were encoded on the minus strand with significant imbalance in distribution. Additionally, 28 tRNA genes, three rRNA genes, 16 introns and 18 putative open reading frames (ORFs) were annotated. Eight ORFs arranged in a row occupied about 18 kbp between psaA and atpI genes, and 16 introns (14 group I introns and 2 group II introns) were annotated in nine genes. Six genes contained nine intronic ORFs. Synteny and rearrangements analysis clearly showed the closest relationships between Chaetophora sp. and C. lobata. Substitution rate estimation indicated that the cpDNA of Chaetophorales was under purifying selection and most species were under similar evolutionary pressure. These findings can help advance research on the taxonomy and phylogeny of the order Chaetophorales.
{"title":"Complete chloroplast genome of the green alga Chaetophora lobata (Chlorophyceae, Chlorophyta): morphological features and phylogenetic and comparative analysis","authors":"Benwen Liu, J. Ge, Huan Zhu, Shuyin Li, Xiaoqi Dong, Guoxiang Liu, Zhengyu Hu","doi":"10.1080/09670262.2021.1923809","DOIUrl":"https://doi.org/10.1080/09670262.2021.1923809","url":null,"abstract":"ABSTRACT Chaetophora lobata is the type species of the polyphyletic genus Chaetophora. Clarification of its species identification, phylogenetic relationships, and plastome characteristics is helpful for taxonomic revisions and evolutionary studies of this genus. This study presents detailed information on morphology, culture, phylogenetic analysis, phylogenomics and comparative genomics of C. lobata. The complete morphological description and phylogenetic analyses based on nuclear rDNA and chloroplast protein-coding genes were robust for the identification of C. lobata. Moreover, de novo sequencing was used to determine the 222 213 bp chloroplast genome, which lacked inverted repeats as in all other members of the Chaetophorales. The chloroplast DNA (cpDNA) of C. lobata was found to be AT-rich (68.2%), consisting of 67 protein-coding genes, among which 62 genes were encoded on the plus strand and five genes were encoded on the minus strand with significant imbalance in distribution. Additionally, 28 tRNA genes, three rRNA genes, 16 introns and 18 putative open reading frames (ORFs) were annotated. Eight ORFs arranged in a row occupied about 18 kbp between psaA and atpI genes, and 16 introns (14 group I introns and 2 group II introns) were annotated in nine genes. Six genes contained nine intronic ORFs. Synteny and rearrangements analysis clearly showed the closest relationships between Chaetophora sp. and C. lobata. Substitution rate estimation indicated that the cpDNA of Chaetophorales was under purifying selection and most species were under similar evolutionary pressure. These findings can help advance research on the taxonomy and phylogeny of the order Chaetophorales.","PeriodicalId":12032,"journal":{"name":"European Journal of Phycology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2021-08-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41926359","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2021-07-23DOI: 10.1080/09670262.2021.1938240
M. M. Barreto Filho, Pierre M. Durand, Nathan E. Andolfato, A. Jordaan, H. Sarmento, I. L. Bagatini
Abstract Reports of programmed cell death (PCD) across the taxonomic spectrum of photosynthetic unicellular organisms raise questions concerning its ecological and evolutionary roles. However, prior to ecological studies or evolutionary interpretations, it is essential to document phenotypic changes associated with PCD at the single-cell level, since death-related responses vary between taxa and within a single taxon depending on environmental stimuli. Here, we report responses to rapidly changing light, temperature and fluctuations in macronutrients in the model selenastracean green microalga Ankistrodesmus densus (Chlorophyta, Chlorophyceae, Sphaeropleales). We used stringent, but environmentally appropriate, conditions of prolonged darkness, nitrogen starvation (4 days), heat (1 h at 44°C) and cold shock (3 h at 2 ± 2°C). PCD phenotypes were examined by ultrastructural changes, phosphatidylserine (PS) externalization and DNA degradation. Flow cytometric Annexin V FITC analyses revealed that darkness and nitrogen-deprived cultures had significantly higher proportions of cells with PS externalization compared with controls (p < 0.05). Heat and cold treatments did not affect PS externalization (p = 0.44 and p = 0.99, respectively). Transmission electron microscopy (TEM) of light-deprived cells demonstrated, among other ultrastructural changes, marked cytoplasmic vacuolization suggesting a subtype of PCD known as vacuolar cell death. Nitrogen-starved cells had less vacuolization but presented more typical ultrastructural markers of PCD such as chromatin condensation and marginalization. In contrast, the more severe heat and cold shock treatments resulted in necrotic-like features. These findings suggest that prolonged darkness and nitrogen starvation induce PCD in a small (8.4 3.5 and 7.42 2.6%, respectively) but significant (p < 0.05) fraction of the A. densus population. Documenting these different death-related phenotypes depending on different environmental inducers is essential for interpreting ecological studies. Furthermore, our data support the hypothesis that autophagic/vacuolar cell death (VCD), which is central to organism homeostasis in plants (Streptophyta), occurs in Chlorophyta. VCD probably arose long before the evolution of multicellularity in plants. HIGHLIGHTS Darkness and nitrogen deprivation induce different programmed cell death markers in Ankistrodesmus densus; Plant vacuolar-like cell death occurs in Chlorophyta; There is crossover between the vacuolar and apoptosis-like death morphotypes.
关于光合单细胞生物的程序性细胞死亡(PCD)的报道提出了关于其生态和进化作用的问题。然而,在生态学研究或进化解释之前,有必要在单细胞水平上记录与PCD相关的表型变化,因为死亡相关的反应在分类群之间和单个分类群内取决于环境刺激而变化。在这里,我们报道了模型硒纲绿色微藻Ankistrodesmus densus(绿藻,绿藻科,球形藻)对快速变化的光、温度和常量营养素波动的响应。我们使用严格但环境适宜的条件,包括长时间黑暗、氮饥饿(4天)、加热(44°C下1小时)和冷休克(2±2°C下3小时)。通过超微结构变化、磷脂酰丝氨酸(PS)外化和DNA降解检测PCD表型。流式细胞仪Annexin V FITC分析显示,暗培养和无氮培养中PS外化细胞比例显著高于对照组(p < 0.05)。冷热处理对PS外化无显著影响(p = 0.44, p = 0.99)。光剥夺细胞的透射电镜(TEM)显示,在其他超微结构变化中,细胞质空泡化明显,提示PCD的一种亚型,即空泡细胞死亡。氮饥饿细胞空泡化程度较低,但呈现出染色质凝聚和边缘化等典型的PCD超微结构标记。相比之下,更严重的热和冷休克治疗导致坏死样特征。上述结果表明,长时间黑暗和氮饥饿对密度白蚁种群PCD的诱导作用虽小,但显著(p < 0.05)(分别为8.3.4 %和7.42 2.6%)。根据不同的环境诱导剂记录这些不同的死亡相关表型对于解释生态学研究至关重要。此外,我们的数据支持了自噬/液泡细胞死亡(VCD)的假设,这是植物(链藻类)生物稳态的核心,发生在绿藻中。VCD可能早在植物多细胞进化之前就出现了。黑暗和氮剥夺诱导密度按蚊不同的程序性细胞死亡标记;植物液泡样细胞死亡发生在绿藻中;在空泡型和细胞凋亡样死亡形态之间存在交叉。
{"title":"Programmed cell death in the coccoid green microalga Ankistrodesmus densus Korshikov (Sphaeropleales, Selenastraceae)","authors":"M. M. Barreto Filho, Pierre M. Durand, Nathan E. Andolfato, A. Jordaan, H. Sarmento, I. L. Bagatini","doi":"10.1080/09670262.2021.1938240","DOIUrl":"https://doi.org/10.1080/09670262.2021.1938240","url":null,"abstract":"Abstract Reports of programmed cell death (PCD) across the taxonomic spectrum of photosynthetic unicellular organisms raise questions concerning its ecological and evolutionary roles. However, prior to ecological studies or evolutionary interpretations, it is essential to document phenotypic changes associated with PCD at the single-cell level, since death-related responses vary between taxa and within a single taxon depending on environmental stimuli. Here, we report responses to rapidly changing light, temperature and fluctuations in macronutrients in the model selenastracean green microalga Ankistrodesmus densus (Chlorophyta, Chlorophyceae, Sphaeropleales). We used stringent, but environmentally appropriate, conditions of prolonged darkness, nitrogen starvation (4 days), heat (1 h at 44°C) and cold shock (3 h at 2 ± 2°C). PCD phenotypes were examined by ultrastructural changes, phosphatidylserine (PS) externalization and DNA degradation. Flow cytometric Annexin V FITC analyses revealed that darkness and nitrogen-deprived cultures had significantly higher proportions of cells with PS externalization compared with controls (p < 0.05). Heat and cold treatments did not affect PS externalization (p = 0.44 and p = 0.99, respectively). Transmission electron microscopy (TEM) of light-deprived cells demonstrated, among other ultrastructural changes, marked cytoplasmic vacuolization suggesting a subtype of PCD known as vacuolar cell death. Nitrogen-starved cells had less vacuolization but presented more typical ultrastructural markers of PCD such as chromatin condensation and marginalization. In contrast, the more severe heat and cold shock treatments resulted in necrotic-like features. These findings suggest that prolonged darkness and nitrogen starvation induce PCD in a small (8.4 3.5 and 7.42 2.6%, respectively) but significant (p < 0.05) fraction of the A. densus population. Documenting these different death-related phenotypes depending on different environmental inducers is essential for interpreting ecological studies. Furthermore, our data support the hypothesis that autophagic/vacuolar cell death (VCD), which is central to organism homeostasis in plants (Streptophyta), occurs in Chlorophyta. VCD probably arose long before the evolution of multicellularity in plants. HIGHLIGHTS Darkness and nitrogen deprivation induce different programmed cell death markers in Ankistrodesmus densus; Plant vacuolar-like cell death occurs in Chlorophyta; There is crossover between the vacuolar and apoptosis-like death morphotypes.","PeriodicalId":12032,"journal":{"name":"European Journal of Phycology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2021-07-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1080/09670262.2021.1938240","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"44436718","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2021-07-03DOI: 10.1080/09670262.2020.1814423
A. Prazukin, N. Shadrin, D. Balycheva, Yu. K. Firsov, Raisa Lee, E. Anufriieva
ABSTRACT Cladophora spp. constantly or periodically form floating and benthic mats in Crimean hypersaline lakes and lagoons. In 2017–2018, characteristics of the Cladophora mats and the microalgae on Cladophora filaments were studied employing field research and microscopy. The whole Cladophora mat has a vertical structure, including the upper and lower layers of the floating mat and benthic mat. In total, 50 species of microalgae were found: 40 of them belonged to Bacillariophyta (Bacillariophyceae and Mediophyceae), two to Haptophyta (Coccolithophyceae), four to Miozoa (Dinophyceae), one to Chlorophyta (Zygnematophyceae) and three to Cyanobacteria (Cyanophyceae). Floating layers of the mat differed significantly in species composition from the benthic mat. The total abundance of microalgae and their biomass on Cladophora (per unit area of filaments) varied widely within sampling sites from 3.79 × 106 to 5.04 × 108 cells m–2 and 2.6 to 2197.8 mg m–2. The total mass of microalgae achieved more than 32% of the mass of Cladophora, averaging 7.7% (standard deviation = 13.3).
{"title":"Cladophora spp. (Chlorophyta) modulate environment and create a habitat for microalgae in hypersaline waters","authors":"A. Prazukin, N. Shadrin, D. Balycheva, Yu. K. Firsov, Raisa Lee, E. Anufriieva","doi":"10.1080/09670262.2020.1814423","DOIUrl":"https://doi.org/10.1080/09670262.2020.1814423","url":null,"abstract":"ABSTRACT Cladophora spp. constantly or periodically form floating and benthic mats in Crimean hypersaline lakes and lagoons. In 2017–2018, characteristics of the Cladophora mats and the microalgae on Cladophora filaments were studied employing field research and microscopy. The whole Cladophora mat has a vertical structure, including the upper and lower layers of the floating mat and benthic mat. In total, 50 species of microalgae were found: 40 of them belonged to Bacillariophyta (Bacillariophyceae and Mediophyceae), two to Haptophyta (Coccolithophyceae), four to Miozoa (Dinophyceae), one to Chlorophyta (Zygnematophyceae) and three to Cyanobacteria (Cyanophyceae). Floating layers of the mat differed significantly in species composition from the benthic mat. The total abundance of microalgae and their biomass on Cladophora (per unit area of filaments) varied widely within sampling sites from 3.79 × 106 to 5.04 × 108 cells m–2 and 2.6 to 2197.8 mg m–2. The total mass of microalgae achieved more than 32% of the mass of Cladophora, averaging 7.7% (standard deviation = 13.3).","PeriodicalId":12032,"journal":{"name":"European Journal of Phycology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2021-07-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1080/09670262.2020.1814423","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"49305171","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2021-06-28DOI: 10.1080/09670262.2021.1914863
T. Lajeunesse, J. Wiedenmann, P. Casado-Amezúa, I. D’Ambra, Kira E. Turnham, M. R. Nitschke, Clinton A. Oakley, S. Goffredo, C. Spano, V. Cubillos, S. Davy, D. Suggett
ABSTRACT The dinoflagellate family Symbiodiniaceae comprises numerous genera and species with large differences in diversity, ecology and geographic distribution. An evolutionarily divergent lineage common in temperate symbiotic cnidarians and designated in the literature by several informal names including ‘temperate–A’, AI, Phylotype A´ (A-prime) and ‘Mediterranean A’, is here assigned to the genus Philozoon. This genus was proposed by Geddes (1882) in one of the earliest papers that recognized ‘yellow cells’ as distinct biological entities separate from their animal and protist hosts. Using phylogenetic data from nuclear (rDNA), chloroplast (cp23S) and mitochondrial genes (cob and cox1), as well as morphology (cell size), ecological traits (host affinity) and geographic distributions, we emend the genus Philozoon Geddes and two of its species, P. medusarum and P. actiniarum, and describe six new species. Each symbiont species exhibits high host fidelity for particular species of sea anemone, soft coral, stony coral and a rhizostome jellyfish. Philozoon is most closely related to Symbiodinium (formerly Clade A), but, unlike its tropical counterpart, occurs in hosts in shallow temperate marine habitats in northern and southern hemispheres including the Mediterranean Sea, north-eastern Atlantic Ocean, eastern Australia, New Zealand and Chile. The existence of a species-diverse lineage adapted to cnidarian hosts living in high latitude habitats with inherently wide fluctuations in temperature calls further attention to the ecological and biogeographic reach of the Symbiodiniaceae. HIGHLIGHTS A dinoflagellate genus symbiotic with temperate invertebrates is characterized and named using a discarded taxonomic term revived from the golden age of Natural Historians. The work highlights how animal–algal mutualisms are evolved to thrive under a broad range of environmental conditions.
共生鞭毛科(dioflagellate family Symbiodiniaceae)由众多属、种组成,在多样性、生态和地理分布上存在较大差异。在温带共生刺胞动物中常见的进化上不同的谱系,在文献中被指定为几个非正式名称,包括“温带A”,AI, A ' (A-prime)和“地中海A”,这里被分配给Philozoon属。这个属是由Geddes(1882)在最早的一篇论文中提出的,该论文认为“黄细胞”是与动物和原生宿主分离的独特生物实体。利用核(rDNA)、叶绿体(cp23S)和线粒体基因(cob和cox1)的系统发育数据,以及形态(细胞大小)、生态性状(寄主亲和力)和地理分布,对Philozoon Geddes属及其两个种P. medusarum和P. actiniarum进行了修订,并描述了6个新种。每种共生体物种对特定种类的海葵、软珊瑚、石珊瑚和根茎水母都有很高的寄主保真度。Philozoon与symbiodiium(以前的进化门A)关系最密切,但与热带的同类物种不同,它的宿主生活在北半球和南半球的浅温带海洋栖息地,包括地中海、大西洋东北部、澳大利亚东部、新西兰和智利。在高纬度、温度波动较大的生境中,存在一种适应刺胞动物宿主的物种多样性谱系,这进一步引起了人们对共生体科生态和生物地理范围的关注。与温带无脊椎动物共生的鞭毛属被表征并使用从自然历史学家的黄金时代复兴的废弃分类术语命名。这项工作强调了动物-藻类的共生关系是如何在广泛的环境条件下进化而茁壮成长的。
{"title":"Revival of Philozoon Geddes for host-specialized dinoflagellates, ‘zooxanthellae’, in animals from coastal temperate zones of northern and southern hemispheres","authors":"T. Lajeunesse, J. Wiedenmann, P. Casado-Amezúa, I. D’Ambra, Kira E. Turnham, M. R. Nitschke, Clinton A. Oakley, S. Goffredo, C. Spano, V. Cubillos, S. Davy, D. Suggett","doi":"10.1080/09670262.2021.1914863","DOIUrl":"https://doi.org/10.1080/09670262.2021.1914863","url":null,"abstract":"ABSTRACT The dinoflagellate family Symbiodiniaceae comprises numerous genera and species with large differences in diversity, ecology and geographic distribution. An evolutionarily divergent lineage common in temperate symbiotic cnidarians and designated in the literature by several informal names including ‘temperate–A’, AI, Phylotype A´ (A-prime) and ‘Mediterranean A’, is here assigned to the genus Philozoon. This genus was proposed by Geddes (1882) in one of the earliest papers that recognized ‘yellow cells’ as distinct biological entities separate from their animal and protist hosts. Using phylogenetic data from nuclear (rDNA), chloroplast (cp23S) and mitochondrial genes (cob and cox1), as well as morphology (cell size), ecological traits (host affinity) and geographic distributions, we emend the genus Philozoon Geddes and two of its species, P. medusarum and P. actiniarum, and describe six new species. Each symbiont species exhibits high host fidelity for particular species of sea anemone, soft coral, stony coral and a rhizostome jellyfish. Philozoon is most closely related to Symbiodinium (formerly Clade A), but, unlike its tropical counterpart, occurs in hosts in shallow temperate marine habitats in northern and southern hemispheres including the Mediterranean Sea, north-eastern Atlantic Ocean, eastern Australia, New Zealand and Chile. The existence of a species-diverse lineage adapted to cnidarian hosts living in high latitude habitats with inherently wide fluctuations in temperature calls further attention to the ecological and biogeographic reach of the Symbiodiniaceae. HIGHLIGHTS A dinoflagellate genus symbiotic with temperate invertebrates is characterized and named using a discarded taxonomic term revived from the golden age of Natural Historians. The work highlights how animal–algal mutualisms are evolved to thrive under a broad range of environmental conditions.","PeriodicalId":12032,"journal":{"name":"European Journal of Phycology","volume":null,"pages":null},"PeriodicalIF":2.4,"publicationDate":"2021-06-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://sci-hub-pdf.com/10.1080/09670262.2021.1914863","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"45453756","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}