Current Articles

Research Paper
Biodiversity of freshwater ciliates (Protista, Ciliophora) in the Lake Weishan Wetland, China: the state of the art
Zhe Wang, Yong Chi, Tao Li, Wenya Song, Yunfeng Wang, Tong Wu, Gongaote Zhang, Yujie Liu, Honggang Ma, Weibo Song, Khaled A. S. Al-Rasheid, Alan Warren, Borong Lu
2022, 4(4): 429-451. doi: 10.1007/s42995-022-00154-x
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Abstract:
Ciliates are core components of the structure of and function of aquatic microbial food webs. They play an essential role in the energy flow and material circulation within aquatic ecosystems. However, studies on the taxonomy and biodiversity of freshwater ciliates, especially those in wetlands in China are limited. To address this issue, a project to investigate the freshwater ciliates of the Lake Weishan Wetland, Shandong Province, commenced in 2019. Here, we summarize our findings to date on the diversity of ciliates. A total of 187 ciliate species have been found, 94 of which are identified to species-level, 87 to genus-level, and six to family-level. These species show a high morphological diversity and represent five classes, i.e., Heterotrichea, Litostomatea, Prostomatea, Oligohymenophorea, and Spirotrichea. The largest number of species documented are oligohymenophoreans. A comprehensive database of these ciliates, including morphological data, gene sequences, microscope slide specimens and a DNA bank, has been established. In the present study, we provide an annotated checklist of retrieved ciliates as well as information on the sequences of published species. Most of these species are recorded in China for the first time and more than 20% are tentatively identified as new to science. Additionally, an investigation of environmental DNA revealed that the ciliate species diversity in Lake Weishan Wetland is higher than previously supposed.
Integrative studies on three new freshwater Amphileptus species (Ciliophora, Pleurostomatida) discovered in northern China
Gongaote Zhang, Yalan Sheng, Yujie Liu, Xiao Cao, Saleh A. Al-Farraj, Peter Vďačný, Hongbo Pan
2022, 4(4): 452-470. doi: 10.1007/s42995-022-00143-0
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Abstract:
The morphology and molecular phylogeny of freshwater pleurostomatid ciliates are insufficiently explored. In the present study, we investigated three new Amphileptus species discovered in Lake Weishan and its vicinity, northern China, using standard alpha-taxonomic methods. Amphileptus paracarchesii sp. nov. is characterized by a lateral fossa (groove) in the posterior body portion, four macronuclear nodules, contractile vacuoles distributed along the dorsal margin, and 4–6 left and 44–50 right somatic kineties. Amphileptus pilosus sp. nov. differs from congeners by having 4–14 macronuclear nodules, numerous contractile vacuoles scattered throughout the cytoplasm, and 22–31 left and 35–42 right somatic kineties. Amphileptus orientalis sp. nov. is characterized by two ellipsoidal macronuclear nodules, three ventral contractile vacuoles, and about four left and 31–35 right somatic kineties. Phylogenetic analyses of nuclear small subunit ribosomal DNA (SSU rDNA) sequences indicate that the family Amphileptidae might be monophyletic while the genus Amphileptus is paraphyletic, as Pseudoamphileptus macrostoma robustly groups with Amphileptus sp. Although deep phylogenetic relationships of amphileptids are poorly resolved, multiple well-delimited species groups are recognizable within the genus Amphileptus.
Phylogeny of the anaerobic ciliate genus Sonderia (Protista: Ciliophora: Plagiopylea), including the description of three novel species and a brief revision of the genus
Ran Li, Wenbao Zhuang, Xiaochen Feng, Saleh A. Al-Farraj, Alan Warren, Xiaozhong Hu
2022, 4(4): 493-512. doi: 10.1007/s42995-022-00142-1
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Abstract:
Anaerobic protists in general, and ciliates in particular, are important components of anoxic or hypoxic environments, however, their diversity remains underestimated. Sonderia is a poorly studied genus that is distributed worldwide and is commonly found in anaerobic environments. In the present study, the taxonomy and phylogeny of three new species, namely Sonderia aposinuata sp. nov., Sonderia paramacrochilus sp. nov. and Sonderia steini sp. nov., collected from China, were investigated based on microscopic observations and SSU rRNA gene sequencing methods. Sonderia aposinuata sp. nov. is diagnosed mainly by having a relatively large body size, a crescent-shaped oral opening, numerous slender extrusomes, one suture on the ventral side and two on the dorsal side, and a buccal cavity that occupies the anterior third of the cell. Sonderia paramacrochilus sp. nov. closely resembles S. macrochilus but differs mainly by its oral opening being located closer to the anterior cell margin and its spindle-shaped extrusomes. Sonderia steini sp. nov. is a freshwater species that can be recognized by its shallow buccal cavity, sparsely distributed rod-shaped extrusomes, and having 68–79 monokinetidal somatic kineties that form sutures on both sides of the body. Phylogenetic analyses based on small subunit ribosomal RNA (SSU rRNA) gene sequence data support the monophyly of the family Sonderiidae, however, Sonderia is paraphyletic. The genus Sonderia is briefly revised and a key to the identification of species belonging to this genus is supplied.
Ontogenesis and systematic position of a new hypotrichous ciliate, Chaetospira sinica sp. nov., with an improved diagnosis of the poorly defined family Chaetospiridae Jankowski, 1985 (Protozoa, Ciliophora, Hypotrichia)
Wenya Song, Xiaotian Luo, Yong Chi, Saleh A. Al-Farraj, Chen Shao
2022, 4(4): 513-526. doi: 10.1007/s42995-022-00146-x
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Abstract:
Ciliates are unique single-celled organisms that play important roles in ecological, environmental, evolutionary, and ontogenetic research. In the present study, phylogenetic analyses based on 18S rRNA gene sequence data reveal that Chaetospira sinica sp. nov. clusters with Stichotricha aculeata with strong to full support (97% ML, 1.00 BI), but is not closely related to members of Spirofilidae Gelei, 1929 to which Chaetospira and Stichotricha have previously been assigned. Phylogenetic analyses, together with morphological and morphogenetic data from Chaetospira sinica sp. nov., support the validity of family Chaetospiridae Jankowski, 1985. Chaetospira and Stichotricha are here assigned to the family Chaetospiridae, the improved diagnosis of which is as follows: non-dorsomarginalian Hypotrichia with flask-shaped body; oral region extending along narrow anterior neck region; lorica usually present; two ventral and two marginal cirral rows, all distinctly spiraled or obliquely curved; pretransverse and transverse cirri absent. The basic morphogenetic features in C. sinica sp. nov. can be summarized as: (1) the oral primordium for the opisthe develops de novo and the parental adoral zone is completely retained by the proter; (2) all ventral cirral anlagen and marginal anlagen developed intrakinetally; (3) three dorsal kineties anlagen formed intrakinetally in each daughter cell; and (4) macronuclear nodules fuse into a single mass. Exconjugant cells were also isolated and their morphologic and molecular data are provided.
Doublets of the unicellular organism Euplotes vannus (Alveolata, Ciliophora, Euplotida): the morphogenetic patterns of the ciliary and nuclear apparatuses associated with cell division
Jinyu Fu, Yong Chi, Xiaoteng Lu, Feng Gao, Saleh A. Al-Farraj, Giulio Petroni, Jiamei Jiang
2022, 4(4): 527-535. doi: 10.1007/s42995-022-00150-1
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Abstract:
Ciliated protists are one of the most diverse and highly differentiated group among unicellular organisms. Doublets occur in ciliates when two cells fuse into a single individual. Doublets contain two major cellular components (either cell in a doublet) and have traditionally been considered as developmental anomalies. Nevertheless, doublets can divide or even conjugate effectively, which may represent dispersal forms of the life stages. In addition, morphogenesis, as an important process in the life cycle, will provide important insights into the complex differentiation mechanism and various physiological phenomena. However, morphogenetic studies focusing on doublets of ciliates are very limited, which has become an obstacle to understand their complete life history. Here we isolated a doublet strain from the marine species Euplotes vannus (Müller, 1786) Diesing, 1850 and investigated its morphogenetic events during asexual reproduction. Our results indicate that: (1) the opisthe's oral primordium develops de novo beneath the cortex; (2) the frontoventral and transverse cirral anlagen, cirrus Ⅰ/1, and marginal anlagen in both dividers develop de novo separately; (3) the dorsal kinety anlagen, the three rightmost ones of which produce three caudal cirri for the proter, occur within the parental structures in the mid-body region; (4) the opisthe acquires two caudal cirri, one from the end of each two rightmost kineties; and (5) there are two macronuclei and one micronucleus in the doublet and they divide amitotically and mitotically, respectively. Finally, we speculate that this special differentiation may be an adaptive form to adverse environments.
Hypotrichidium tisiae (Gelei, 1929) Gelei, 1954: a unique hypotrichid ciliate having a highly specialized developmental pattern during binary division
Xiaotian Luo, Jie Huang, Honggang Ma, Yujie Liu, Xiaoteng Lu, William A. Bourland
2022, 4(4): 536-550. doi: 10.1007/s42995-022-00148-9
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Abstract:
In sharp contrast to their pelagic relatives, the oligotrichs, the overwhelming majority of hypotrich ciliates inhabit the benthos. Only a few species, including those of the genus Hypotrichidium Ilowaisky, 1921, have adapted to a planktonic lifestyle. The ontogenetic mode of the highly differentiated ciliate, Hypotrichidium tisiae (Gelei, 1929) Gelei, 1954, is unknown. In this study, the interphase morphology and the ontogenetic process of this species are investigated. Accordingly, the previously unidentified ciliary pattern of Hypotrichidium is redefined. The main morphogenetic features are as follows: (1) The parental adoral zone of membranelles is inherited completely by the proter and the oral primordium of the opisthe arises in a deep pouch. (2) Five frontoventral cirral anlagen (FVA) are formed: FVA Ⅰ contributes to the single frontal cirrus, FVA Ⅱ–Ⅳ generate three frontoventral cirral rows, FVA Ⅴ migrates and forms postoral ventral cirri. (3) All marginal cirral row anlagen develop de novo: each of the two left anlagen forms a single cirral row, while the single right anlage fragments into anterior and posterior parts. (4) Two dorsal kinety anlagen occur de novo, with the right one fragmenting to form kineties 2 and 3. (5) Two long caudal cirral rows are formed at the ends of dorsal kineties 1 and 3. On the basis of the morphogenetic features and phylogenetic analyses, the assignment of Hypotrichidium to the family Spirofilidae Gelei, 1929 within Postoralida is supported. The establishment of separate families for the slender "tubicolous" spirofilids and the highly helical spirofilids is also validated.
Ultrastructure of Diophrys appendiculata and new systematic consideration of the euplotid family Uronychiidae (Protista, Ciliophora)
Jingyi Dong, Yujie Liu, Jiyang Ma, Honggang Ma, Thorsten Stoeck, Xinpeng Fan
2022, 4(4): 551-568. doi: 10.1007/s42995-022-00153-y
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Abstract:
The ultrastructure of ciliates carries important cytological, taxonomical, and evolutionary signals for these single-celled eukaryotic organisms. However, little ultrastructural data have been accumulated for most ciliate groups with systematic problems. In the present work, a well-known marine uronychiid, Diophrys appendiculata, was investigated using electron microscopy and a comparison with, and a discussion considering, phylogenetic analyses were made. The new findings primarily show that: (ⅰ) this species lacks the typical alveolar plate, bears cortical ampule-like extrusomes, and has microtubular triads in the dorsal pellicle, and thus exhibits some ultrastructural features in common with most of its previously studied congeners; (ⅱ) each adoral membranelle before the level of frontal cirrus Ⅱ/2 contains three rows of kinetosomes and each membranelle after the level of frontal cirrus Ⅱ/2 contains four rows, which might be related with morphogenesis and could be considered as a distinctive character of Diophrys; (ⅲ) some structural details of the buccal field, such as the extra-pellicular fibrils, pellicle, pharyngeal disks and microtubular sheet, were documented. In addition, based on the ultrastructural comparison of representatives, we discuss the differentiation between the subfamilies Diophryinae and Uronychiinae. A hypothetical systematic relationship of members in the order Euplotida based on a wide range of data is also provided.
New considerations on the phylogeny of Sessilida (Protista: Ciliophora: Peritrichia) based on multiple-gene information, with emphasis on colonial taxa
Zhe Wang, Xiaoting Feng, Lifang Li, Khaled A. S. Al-Rasheid, Alan Warren, Chundi Wang, Zemao Gu
2022, 4(4): 569-583. doi: 10.1007/s42995-022-00155-w
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Abstract:
The subclass Peritrichia, containing two orders Sessilida and Mobilida, is a major group of ciliates with worldwide distribution and high species diversity. Several studies have investigated the phylogeny of peritrichs; however, the evolutionary relationships and classification of some families and genera within the Sessilida remain unclear. In the present study, we isolated and identified 22 peritrich populations representing four families and six genera and obtained 64 rDNA sequences to perform phylogenetic analyses and assess their systematic relationships. Ancestral character reconstruction was also carried out to infer evolutionary routes within the Sessilida. The results indicate: (1) family Vaginicolidae is monophyletic and acquisition of the typical peritrich lorica represents a single evolutionary divergence; (2) core epistylidids evolved from a Zoothamnium-like ancestor and experienced spasmoneme loss during evolution; (3) Campanella clusters with species in the basal clade and shows stable morphological differences with other epistylidids, supporting its assignment to a separate family; (4) the structure of the peristomial lip may be a genus-level character rather than a diagnostic character for discriminating Epistylididae and Operculariidae, thus a redefinition of Operculariidae should be carried out when more species have been investigated; (5) some characters, such as lifestyle (solitary or colonial), spasmoneme and living habit (sessile or free-swimming), evolved repeatedly among sessilids indicating that species with non-contractile stalks or that are free-swimming have multiple evolutionary routes and might derive from any sessilid lineage without a lorica. The close phylogenetic relationships of some morphologically distinct sessilids imply that the diagnoses of some genera and families should be improved.
Group-specific functional patterns of mitochondrion-related organelles shed light on their multiple transitions from mitochondria in ciliated protists
Zhicheng Chen, Jia Li, Dayana E. Salas-Leiva, Miaoying Chen, Shilong Chen, Senru Li, Yanyan Wu, Zhenzhen Yi
2022, 4(4): 609-623. doi: 10.1007/s42995-022-00147-w
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Abstract:
Adaptations of ciliates to hypoxic environments have arisen independently several times. Studies on mitochondrion-related organelle (MRO) metabolisms from distinct anaerobic ciliate groups provide evidence for understanding the transitions from mitochondria to MROs within eukaryotes. To deepen our knowledge about the evolutionary patterns of ciliate anaerobiosis, mass-culture and single-cell transcriptomes of two anaerobic species, Metopus laminarius (class Armophorea) and Plagiopyla cf. narasimhamurtii (class Plagiopylea), were sequenced and their MRO metabolic maps were compared. In addition, we carried out comparisons using publicly available predicted MRO proteomes from other ciliate classes (i.e., Armophorea, Litostomatea, Muranotrichea, Oligohymenophorea, Parablepharismea and Plagiopylea). We found that single-cell transcriptomes were similarly comparable to their mass-culture counterparts in predicting MRO metabolic pathways of ciliates. The patterns of the components of the MRO metabolic pathways might be divergent among anaerobic ciliates, even among closely related species. Notably, our findings indicate the existence of group-specific functional relics of electron transport chains (ETCs). Detailed group-specific ETC functional patterns are as follows: full oxidative phosphorylation in Oligohymenophorea and Muranotrichea; only electron-transfer machinery in Armophorea; either of these functional types in Parablepharismea; and ETC functional absence in Litostomatea and Plagiopylea. These findings suggest that adaptation of ciliates to anaerobic conditions is group-specific and has occurred multiple times. Our results also show the potential and the limitations of detecting ciliate MRO proteins using single-cell transcriptomes and improve the understanding of the multiple transitions from mitochondria to MROs within ciliates.
Review
The widely reported but poorly studied ciliate family Folliculinidae (Protozoa, Ciliophora, Heterotrichea): a revision with notes on its taxonomy, morphology and phylogenetic relationships
Tingting Ye, Yaohan Jiang, Shuchang Chen, Yixiang Xu, Lifang Li, Mann Kyoon Shin, Xiangrui Chen
2022, 4(4): 471-492. doi: 10.1007/s42995-022-00152-z
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Abstract:
Ciliates of the heterotrich family Folliculinidae are widespread in various habitats and are distinguished by their transparent loricae of various shapes, conspicuous peristomial lobes, and dimorphic life cycles. They usually attach firmly to the surface of substrates, feed on bacteria and microalgae, and play a significant role in energy flow and material cycling in the microbial food web. However, little is known regarding their biodiversity and systematics. In this work, we establish the terminology of the family Folliculinidae and select six crucial features for genus recognition. Based on previous studies, we revise the classification of Folliculinidae, supply improved diagnoses for each of the 33 folliculinid genera, and provide a key to their identification. Moreover, phylogenetic analyses based on small subunit ribosomal DNA (SSU rDNA) sequences revealed that the family is monophyletic and comprises two subclades (subclades Ⅰ Ⅱ) which can be identified by the flexibility of their peristomial lobes and the sculpturing of their necks. Furthermore, we investigate the evolutionary relationships of folliculinids using the six chosen generic features.
The micronuclear histone H3 clipping in the unicellular eukaryote Tetrahymena thermophila
Fan Wei, Bo Pan, Jinghan Diao, Yuanyuan Wang, Yalan Sheng, Shan Gao
2022, 4(4): 584-594. doi: 10.1007/s42995-022-00151-0
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Abstract:
Clipping of the histone H3 N-terminal tail has been implicated in multiple fundamental biological processes for a growing list of eukaryotes. H3 clipping, serving as an irreversible process to permanently remove some post-translational modifications (PTMs), may lead to noticeable changes in chromatin dynamics or gene expression. The eukaryotic model organism Tetrahymena thermophila is among the first few eukaryotes that exhibits H3 clipping activity, wherein the first six amino acids of H3 are cleaved off during vegetative growth. Clipping only occurs in the transcriptionally silent micronucleus of the binucleated T. thermophila, thus offering a unique opportunity to reveal the role of H3 clipping in epigenetic regulation. However, the physiological functions of the truncated H3 and its protease(s) for clipping remain elusive. Here, we review the major findings of H3 clipping in T. thermophila and highlight its association with histone modifications and cell cycle regulation. We also summarize the functions and mechanisms of H3 clipping in other eukaryotes, focusing on the high diversity in terms of protease families and cleavage sites. Finally, we predict several protease candidates in T. thermophila and provide insights for future studies.
A practical reference for studying meiosis in the model ciliate Tetrahymena thermophila
Miao Tian, Xia Cai, Yujie Liu, Mingmei Liucong, Rachel Howard-Till
2022, 4(4): 595-608. doi: 10.1007/s42995-022-00149-8
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Abstract:
Meiosis is a critical cell division program that produces haploid gametes for sexual reproduction. Abnormalities in meiosis are often causes of infertility and birth defects (e.g., Down syndrome). Most organisms use a highly specialized zipper-like protein complex, the synaptonemal complex (SC), to guide and stabilize pairing of homologous chromosomes in meiosis. Although the SC is critical for meiosis in many eukaryotes, there are organisms that perform meiosis without a functional SC. However, such SC-less meiosis is poorly characterized. To understand the features of SC-less meiosis and its adaptive significance, the ciliated protozoan Tetrahymena was selected as a model. Meiosis research in Tetrahymena has revealed intriguing aspects of the regulatory programs utilized in its SC-less meiosis, yet additional efforts are needed for obtaining an in-depth comprehension of mechanisms that are associated with the absence of SC. Here, aiming at promoting a wider application of Tetrahymena for meiosis research, we introduce basic concepts and core techniques for studying meiosis in Tetrahymena and then suggest future directions for expanding the current Tetrahymena meiosis research toolbox. These methodologies could be adopted for dissecting meiosis in poorly characterized ciliates that might reveal novel features. Such data will hopefully provide insights into the function of the SC and the evolution of meiosis from a unique perspective.