Research Article |
Corresponding author: Hiroki Kise ( hkm11sea@yahoo.co.jp ) Academic editor: Bert W. Hoeksema
© 2023 Hiroki Kise, Miyuki Nishijima, Akira Iguchi, Junpei Minatoya, Hiroyuki Yokooka, Yuji Ise, Atsushi Suzuki.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Kise H, Nishijima M, Iguchi A, Minatoya J, Yokooka H, Ise Y, Suzuki A (2023) A new hexactinellid-sponge-associated zoantharian (Porifera, Hexasterophora) from the northwestern Pacific Ocean. ZooKeys 1156: 71-85. https://doi.org/10.3897/zookeys.1156.96698
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Symbiotic associations between zoantharians and sponges can be divided into two groups: those that associate with Demospongiae and those that associate with Hexactinellida. Parachurabana shinseimaruae Kise, gen. nov. et sp. nov., a new genus and a new species of Hexactinellida-associated zoantharian from Japanese waters, is described. It is characterized by a combination of the following: i) its host hexactinellid sponge, ii) very flat polyps, iii) cteniform endodermal marginal muscles, and iv) characteristic mutations in three mitochondrial regions (including a unique 26-bp deletion in 16S ribosomal DNA) and three nuclear regions. Parachurabana shinseimaruae Kise, gen. nov. et sp. nov. is the third genus in the family Parazoanthidae that is reported to be associated with Hexasterophora sponges. Although specimens have so far only been collected on Takuyo-Daigo Seamount off Minami-Torishima Island in Japan, unidentified zoantharians of similar description have been reported from the waters around Australia, indicating that the species might be widespread across the Pacific.
Glass sponge, Hexasterophora, host specificity, molecular phylogeny, symbiosis
The family Parazoanthidae Delage & Hérouard, 1901 comprises 16 genera and more than 50 species (
Recently, we collected a single specimen of parazoanthid associated with a hexactinellid sponge in the family Farreidae Gray, 1872 during a benthic survey of the Takuyo-Daigo Seamount in the western Pacific Ocean. On the basis of molecular phylogenetic analyses combined with morphological and ecological data, we formally describe it here as the new species Parachurabana shinseimaruae gen. nov. et sp. nov. (authored by Kise).
A single specimen was collected on 19 June 2020 by using a remotely operated submersible on Takuyo-Daigo Seamount off southwestern Minami-Torishima Island in the northwestern Pacific Ocean during a cruise aboard the RV Shinsei-maru. Photographs of the specimen were taken in situ for gross external morphological observation. The collected specimen was fixed in 99.5% EtOH and stored at –80 °C.
Genomic DNA was extracted from the tissue of the holotype specimen using a spin-column DNeasy Blood and Tissue Extraction Kit (Qiagen, Hilden, Germany) following the manufacture’s protocol. PCR amplification using Takara Ex Taq DNA Polymerase Hot Start Version (TaKaRa Bio, Inc., Shiga, Japan) was conducted for mitochondrial cytochrome c oxidase subunit I (COI) with jgLCO1490 and jgHCO2198 (
All PCR products were purified with ExoSAP-IT™ PCR Product Cleanup Reagent (Thermo Fisher Scientific, Waltham, MA, USA) at 37 °C for 15 min followed by 80 °C for 15 min. Purified PCR products were sequenced by Macrogen Japan, Inc. (Kyoto, Japan). Obtained sequences in this study were deposited in GenBank (Suppl. material
Bidirectional sequences were assembled and edited in Geneious v. 10.2.3 (
Phylogenetic analyses were performed on the concatenated dataset using maximum likelihood (ML) and Bayesian inference (BI). ModelTest-NG v. 0.1.6 (
ITS-rDNA has been considered as a useful marker to delineate species in Zoantharia (
External morphological characters of the preserved specimen were examined using in-situ images and a dissecting microscope. Internal morphological characters were examined by using histological sections; 10–15 µm serial sections were made with a microtome (LEICA RM2145; Leica, Germany) and stained with haematoxylin and eosin after decalcification with Morse solution for 48 h (1:1 vol; 20% citric acid: 50% formic acid) and desilication with 20% hydrofluoric acid for 18–24 h. Classification of marginal muscle shapes followed the scheme described by
CMNH Coastal Branch of the Natural History Museum and Institute, Chiba, Japan;
NSMT National Science Museum, Tsukuba, Ibaraki, Japan;
RMNH Rijksmuseum van Natuurlijke Historie (now at the Naturalis Biodiversity Center), Leiden, the Netherlands;
RUMF Ryukyu University Museum (Fujukan), University of the Ryukyus, Okinawa, Japan.
Order Zoantharia Rafinesque, 1815
Suborder Macrocnemina Haddon & Shackleton, 1891
Parachurabana shinseimaruae Kise sp. nov. by original designation.
Parazoanthidae with symbiotic relationship with farreid sponges. Polyp cylindrical and flat when preserved. Preserved polyps 0.5–1.0 mm in height, 0.5–3.0 mm in diameter. Azooxanthellate. Cteniform endodermal marginal muscle.
Parachurabana gen. nov. is differentiated from other sponge-associated parazoanthids based on a combination of host-sponge identity and morphological features. Parachurabana gen. nov. is easily distinguished from the genera Bergia, Parazoanthus, and Umimayanthus by its association with hexactinellid sponges, as the three other genera are associated with Demospongiae sponges. In Hexactinellida-sponge-associated Parazoanthidae genera, the association with subclass Amphidiscophora differentiates Parachurabana gen. nov. from Isozoanthus. Marginal muscle morphology differentiates Parachurabana gen. nov. (cteniform endodermal marginal muscles) from Vitrumanthus (cyclically transitional marginal muscles). Parachurabana gen. nov. can be distinguished from Churabana by polyp size, as Parachurabana gen. nov. has very flat polyps when preserved (0.5–1.0 mm in height, 0.5–3.0 mm in diameter) in comparison to Churabana (3.0–4.0 mm in height, 2.8–4.0 mm in diameter). In the16S-rDNA region, Parachurabana gen. nov. is characterized by a unique deletion of 26 bp (positions 136–150 and 168–178 in our alignment) (Suppl. material
Parachurabana alludes to its morphological similarities to Churabana. The Prefix “para” is a Greek word meaning “resembling.”
Holotype. NSMT-Co 1819, Takuyo-Daigo Seamount off southwestern Minami-Torishima Island, 23°23'N, 153°04'E, 935 m depth, coll. RV Shinsei-maru, 19 June 2020, fixed in 99.5% ethanol.
Churabana kuroshioae RUMF-ZG-04447 (holotype), collected from near Iejima Island, Motobu, Okinawa, Japan by T. Higashiji, 02 Mar. 2018. Vitrumanthus schrieri RMNH.COEL.42429 (holotype), collected from SubStation, Curaçao by B.W. Hoeksema, 31 Mar. 2014. Vitrumanthus vanderlandi RMNH.COEL.42623 (holotype), Cape Verde Islands, São Tiago, Ilheus Rombos east of Cima by RV HNIMS Tydeman, 24 Aug. 1986. Vitrumanthus oligomyarius CMNH ZG-4785, off Katsuura, Chiba, Japan by A. Tamura, 19 Jan. 2006.
External morphology. Cylindrical polyps that appear solitary and sparsely distributed on the hexactinellid sponge Farrea Bowerbank, 1862 (Fig.
External morphology of Parachurabana shinseimaruae sp. nov. a photographic record from Takuyo-Daigo Seamount off southwestern Minami-Torishima Island b–d NSMT-Co 1819 a living polyps on a hexactinellid sponge Farrea sp. b preserved specimen c close-up image of a single preserved polyp d close-up, side-view image of a single preserved polyp attached to a hexactinellid sponge Farrea sp. Scale bars: 20 mm (a, b); 1 mm (c, d).
Internal morphology. Zooxanthellae absent. Cteniform endodermal marginal muscle with comb-like mesogleal pleats (Fig.
Images of the internal morphology of Parachurabana shinseimaruae sp. nov. NSMT-Co 1819 a close-up image of cteniform endodermal marginal muscle in a longitudinal polyp section b cross-section at the height of tentacles c cross-section at the height of the actinopharynx. Abbreviations: CEMM, cteniform endodermal marginal muscle; CM, complete mesentery; CW, column wall; DD, dorsal directives; ES, encircling sinus; IM, incomplete mesentery; T, tentacles. Scale bars: 200 µm (a); 500 µm (b, c).
Cnidae. Basitrichs and microbasic b-mastigophores, microbasic p-mastigophores, holotrichs, special b-mastigophores, and spirocysts (See Fig.
Cnidae types and sizes observed in this study. Frequency: relative abundance of cnidae type in decreasing order; numerous, common, occasional, rare. n = number of cnidae measured.
Tissue | Type of cnidae | Length (min–max, mean) | Width (min–max, mean) | Frequency | n |
---|---|---|---|---|---|
Tentacle | Spirocysts | 15.30–32.20, 23.40 | 2.22–4.81, 3.64 | Numerous | 195 |
Basitrichs and microbasic b-mastigophores | 15.31–25.12, 21.54 | 1.61–4.20, 3.38 | Numerous | 67 | |
Holotrichs (L) | 27.97–44.58, 35.29 | 11.63–21.31, 15.20 | Occasional | 11 | |
Column | Special microbasic b-mastigophores | 11.56–16.84, 13.91 | 5.16–8.04, 6.01 | Occasional | 13 |
Holotrich (L) | 28.84–37.84, 32.00 | 10.72–18.72, 15.35 | Common | 18 | |
Actinopharynx | Spirocysts | 18.05–29.02, 23.73 | 2.03–4.62, 3.45 | Numerous | 45 |
Basitrichs and microbasic b-mastigophores | 18.29–27.64, 22.33 | 1.73–4.96, 3.30 | Common | 32 | |
Special microbasic b-mastigophores | 17.88–19.09, 18.48 | 5.69–5.73, 5.71 | Rare | 2 | |
Holotrichs (L) | 38.33–48.65, 43.00 | 11.08–17.51, 13.96 | Rare | 3 | |
Mesenterial filaments | Spirocysts | 19.31–32.17, 24.76 | 2.26–4.81, 3.40 | Occasional | 11 |
Bastrichs and microbasic b-mastigophores | 17.81–27.46, 22.45 | 3.38–4.57, 3.83 | Common | 15 | |
Microbasic p-mastigophores | 14.04–23.25, 19.31 | 5.08–7.51, 5.96 | Occasional | 13 | |
Special microbasic b-mastigophores | 5.84–10.71, 7.79 | 2.68–5.27, 4.21 | Occasional | 11 | |
Holotrichs (L) | 33.13–48.86, 38.93 | 12.39–24.04, 16.39 | Common | 22 |
Cnidae in the tentacles, column, actinopharynx, and mesenterial filaments of the holotype of Parachurabana shinseimaruae sp. nov. Abbreviations: HL, holotrich large; O, basitrichs and microbasic b-mastigophores; SBM, special microbasic b-mastigophores; PM, microbasic p-mastigophores; S, spriocysts.
Northwestern Pacific Ocean: Takuyo-Daigo Seamount off southwestern Minami-Torishima Island at depths of 900–1000 m.
Farrea sp. (Porifera: Hexactinellida)
Both ML and BI phylogenetic analyses using the concatenate dataset indicate that Parachurabana shinseimaruae sp. nov. is basal to the clade containing the genera Bergia, Parazoanthus, and Umimayanthus (Fig.
Parachurabana shinseimaruae sp. nov. has so far only been identified on one seamount off southwestern Minami-Torishima Island. However, Parachurabana shinseimaruae sp. nov. may be distributed across the Pacific Ocean, as several specimens associated with farreid sponges have been observed in Australian waters (M. Ekins personal communication). Although Parachurabana shinseimaruae sp. nov. is morphologically similar to Vitrumanthus schrieri, Parachurabana shinseimaruae sp. nov. and V. schrieri can be separated by marginal muscle (cteniform endodermal marginal muscle vs cyclically transitional marginal muscle). Furthermore, Parachurabana shinseimaruae sp. nov. can be distinguished from Churabana kuroshioae by polyp size (0.5–1.0 mm in height by 0.5–3.0 mm in diameter vs 3.0–4.0 mm in height by 2.8–4.0 mm in diameter).
The species is named after RV Shinsei-maru, as the type specimens were collected by this vessel.
Parachurabana gen. nov. is the third Parazoanthidae genus known to associate with hexasterophoran sponges. Each of these three genera is associated with different hexasterophorans: Parachurabana gen. nov. is known to associate with Farrea (family Farreidae); Churabana with Pararete Ijima, 1927 (Euretidae); and Vitrumanthus with Verrucocoeloidea Reid, 1969 (Euretidae), Cyrtaulon Schulze, 1886 (Sceptrulophora incertae sedis), Aphrocallistes Gray, 1858 (Aphrocallistidae), and Tretochone Reid, 1958 (Euretidae) (
This study was commissioned by the Agency for Natural Resources and Energy in the Ministry of Economy, Trade and Industry, Japan. This study was funded by Japan Organization for Metals and Energy Security (JOGMEC). Computations were partially performed on the NIG supercomputer at the ROIS National Institute of Genetics. We thank Dr Kyoko Yamaoka (AIST) for providing technical support. Comments from Dr James Davis Reimer, Dr Javier Montenegro, and an anonymous reviewer greatly improved this manuscript.
GenBank accession numbers used for phylogenetic analyses in this study
Data type: Accession numbers
Summary of deletions in the alignment of 16S-rDNA that characterize Parachurabana gen. nov.
Data type: figure (eps file)
Bayesian-inference tree based on combined dataset of COI, 12S-rDNA, 16S-rDNA, 18S-rDNA, 28S-rDNA, and ITS-rDNA sequences. Number at nodes represent Bayesian posterior probabilities (>0.95)
Data type: figure (pdf file)
Maximum-likelihood tree based on ITS-rDNA sequences. Number at nodes represent ML bootstrap values (>50% are shown)
Data type: figure (pdf file)