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Non-Blue Haslea Species (Bacillariophyceae: Naviculaceae) in the Benthic Marine Flora of Guam (Mariana Islands, Western Pacific Ocean)

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Non-Blue Haslea Species (Bacillariophyceae: Naviculaceae) in the Benthic Marine Flora of Guam (Mariana Islands, Western Pacific Ocean) Diatom Research ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/tdia20 Non-blue Haslea species (Bacillariophyceae: Naviculaceae) in the benthic marine flora of Guam (Mariana Islands, Western Pacific Ocean). Christopher S. Lobban , Claire O. Perez & Matt P. Ashworth To cite this article: Christopher S. Lobban , Claire O. Perez & Matt P. Ashworth (2020) Non-blue Haslea species (Bacillariophyceae: Naviculaceae) in the benthic marine flora of Guam (Mariana Islands, Western Pacific Ocean)., Diatom Research, 35:2, 163-183, DOI: 10.1080/0269249X.2020.1761887 To link to this article: https://doi.org/10.1080/0269249X.2020.1761887 View supplementary material Published online: 16 Jun 2020. Submit your article to this journal Article views: 10 View related articles View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=tdia20 Diatom Research, 2020 Vol. 35, No. 2, 163–183, https://doi.org/10.1080/0269249X.2020.1761887 Non-blue Haslea species (Bacillariophyceae: Naviculaceae) in the benthic marine flora of Guam (Mariana Islands, Western Pacific Ocean). CHRISTOPHER S. LOBBAN 1∗, CLAIRE O. PEREZ2 & MATT P. ASHWORTH3 1College of Natural & Applied Sciences, University of Guam, Mangilao, GU, USA 2LSAMP Program, College of Natural & Applied Sciences, University of Guam, Mangilao, GU, USA 3UTEX Culture Collection of Algae, Department of Molecular Biosciences, University of Texas, Austin, TX, USA In recent years the taxonomy of Haslea has been in flux. We describe several Haslea taxa from Guam, including four new species, in light of these recent findings. Four delicate, fusiform Haslea species are described from a variety of benthic habitats on coral reefs. These species, H. fusiformis comb. nov. and H. alexanderi, H. apoloniae and H. guahanensis spp. nov. are distinguished by stria density, foramen (‘areola’) shape, and cell size from each other and from similar taxa. A key to all these taxa is provided. In addition, an arcuate species is described as Haslea arculata sp. nov. The presence of a bilayered wall is shown for all these taxa. We compare the morphology of specimens reported as H. howeana from Guam with Navicula tsukamotoi, recently described from Okinawa, and with ‘Navicula cf. howeana’ from Puerto Rico. We provide the first account of the complex cingulum of N. tsukamotoi. We conclude that our specimens match N. tsukamotoi and that H. howeana should be returned to Navicula, but we leave open the question of conspecificity. Keywords: biodiversity, copulae, coral reefs, diatoms, Mariana Islands, Naviculales Introduction (Reid 2012: 52 and pl. 7, Fig. 3) (superb cross-sectional The diatom genus Haslea Simonsen (1974)(formerlyNav- views in Poulin et al. 2004) and the central area in Haslea icula section Fusiformes) is widespread in benthic and is flanked by short accessory ribs or flaps (Schrader 1973, planktonic habitats. It was recently shown to be more Sterrenburg et al. 2015,Lietal.2017),similartothosein diverse than previously thought and to be structurally Pleurosigma and Gyrosigma, but absent in Navicula. related to Pleurosigma W. Smith and Gyrosigma A. Has- Haslea includes a subset of very similar taxa that are sall (Sterrenburg et al. 2015). Morphologically the genus weakly silicified and lack a pseudostauros; Hustedt (1961) was redefined by Sterrenburg et al. (2015) on the basis of a distinguished these on the basis of size and stria densities double-layered wall structure, comprising an inner (basal, (when discernable) plus the rather dubious criterion of geo- ontogenetically earlier), grid-like layer separated from the graphic provenance. The best known is the type species, outer (tegumental) layer of longitudinal strips by parallel, Haslea ostrearia (Gaillon) Simonsen (recently typified by perforated walls they termed saepes. However, Li et al. Poulin et al. 2019), the ‘blue diatom’ coloured by maren- (2017) showed that genetically some species placed in nine in its vacuoles (Nassiri et al. 1998, Pouvreau et al. Haslea, including two of those by Sterrenburg et al. (2015), 2006), which is famous for producing a desirable colour belong in Navicula Bory, and that ‘[the] presence of con- in oysters. Blue pigment is a very distinctive feature of H. tinuous longitudinal strips on the external valve surface is ostrearia, but more recently three new species, H. karada- not a synapomorphy, but rather a homoplastic character gensis Davidovich, Gastineau & Mouget, H. provincialis for Haslea.’ Unfortunately, saepes are difficult to observe, Gastineau, Hansen & Mouget and H. nusantara Mouget, e.g. where suitable breaks in the valves expose them, and Gastineau & Syakti, morphologically very similar but indeed for the species transferred by Li et al. (2017), Ster- molecularly distinct, have been reported to contain a differ- renburg et al. (2015) noted that they had not observed ent blue pigment, as were further, morphologically distinct them. blue Haslea species (Gastineau et al. 2012, 2014a, 2014b, Several other characters differ between Haslea and 2016, Prasetiya et al. 2019). Navicula, though none is synapomorphic for Haslea. For Also in this group is one of the least-known taxa, Nav- example, in Haslea the raphe is overhung by an axial costa, icula fusiformis Grunow [non Navicula fusiformis Ehren- which can be seen twisting over the raphe slit near the apex berg; see VanLandingham 1975]. Grunow (1877) included *Corresponding author. E-mail: [email protected] Associate editor: Koen Sabbe (Received 27 October 2019; accepted 6 April 2020) © 2020 The International Society for Diatom Research Published online 16 Jun 2020 164 Lobban et al. Navicula ostrearia (Gaillon) Turpin in Bory as a vari- Dr. Igersheim was able to loan us several packets con- ety of N. fusiformis, but Sauvageau (1907) treated N. taining residual material from the Honduras Sargassum fusiformis as a variety of N. ostrearia (the latter being samples, though none of it was marked as containing N. the older name), and Hustedt (1961) maintained each at fusiformis. The SEM stubs are stored in the UGUAM species rank. In erecting Haslea, Simonsen (1974) reduced Diatom Herbarium. N. fusiformis to a synonym of H. ostrearia. Apart from Type slides were deposited at the Academy of Natural Grunow’s record from Honduras, Hustedt (1961) noted Sciences of Drexel University, Philadelphia (ANSP). only a few observations by himself from Dubrovnik. The hyaline appearance of the valves in LM makes it difficult to distinguish N. fusiformis from H. ostrearia except by its larger size. Hustedt’s (1961) systematic remarks on the DNA extraction, sequencing and molecular phylogenetic two forms, to which Simonsen (1974) referred in making analysis the synonymy, also note that it is not known whether N. fusiformis has blue pigment. Strains cultured in this study were isolated from wild We found several species of this group in Guam, two material, outlined in Table S1. Strains from Guam were of which were similar to N. fusiformis, and in trying to isolated into f/2 media and grown in a Percival model resolve their identities, we began by seeking unmounted I-36LL incubator at 27°C in a 12:12 h light: dark photope- type material. In this paper, we describe our findings from riod. Harvested material from cultures was stored in pellets these samples and propose four new species of lanceolate made after centrifugation in an Eppendorf 5415C cen- Haslea and a new combination for N. fusiformis. In addi- trifuge (Eppendorf North America, Hauppauge, NY, USA) tion, we investigated a commonly observed arcuate cell for 5 min at 10,000 rpm. For DNA extraction, the QIAGEN with biarcuate raphe branches, which resembled Haslea DNeasy Plant Mini Kit (QIAGEN Sciences, Valencia, Cal- in the outer covering of longitudinal strips. The variety ifornia, USA) was used, with initial cell disruption by of valve shapes within Haslea, as depicted by Sterren- 1.0 mm glass beads in a Mini-Beadbeater (Biospec Prod- burg et al. (2015) could encompass this form, if it had the ucts, Inc, Bartlesville, OK, USA) for 45 sec. PCR-based appropriate valve structure. For this species we were able DNA amplification and di-deoxy Sanger sequencing of to get gene sequences, but most of our attempts to culture small-subunit nuclear rRNA and the chloroplast-encoded Guam Haslea species have not been successful. Finally, a rbcL and psbC markers followed Theriot et al. (2010). species previously identified as Haslea howeana (Hagel- Phylogenetic analysis of the three-gene dataset nuclear- stein) Giffen is common in Guam (Lobban et al. 2012) but encoded small subunit (SSU) rRNA, and plastid-encoded appeared very similar to Haslea tsukamotoi Sterrenburg, rbcL and psbC followed the molecular phylogenetic meth- which Li et al. (2017) transferred to Navicula and also ods outlined in Lobban et al. (2019). The dataset was needs reconsidering in the light of these recent studies. constructed from the pennate dataset used in Sabir et al. (2018), with additional representatives of the Naviculaceae added from GenBank and the strains isolated as above. The Methods final dataset contained 411 taxa of araphid and raphid pen- Raw samples were collected from intertidal and subtidal nate diatoms, using ‘Asterionellopsis socialis HK181’ as reefs around Guam (Table 1) and processed for LM and an outgroup. SSU sequences were aligned using the pro- SEM using standard laboratory protocols (Lobban 2015). gram SSUalign (Nawrocki et al. 2009), with the covariance In brief, samples preserved in formalin were rinsed, boiled model based on the diatoms included in the download, plus with nitric acid and rinsed to neutrality. Drops of the resul- secondary structure models from an additional 23 diatoms tant suspension were dried onto cover slips for LM and found on the CRW website (Cannone et al. 2002). SSU and cellulose nitrate filters for SEM. LM observations were plastid sequences were concatenated into a single matrix, made with a Nikon 80i microscope with differential inter- which is available in the Supplementary Data as Appendix ference contrast and phase contrast illumination, SEM S1.
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