New Insights into Plagiogrammaceae (Bacillariophyta) Based on Multigene Phylogenies and Morphological Characteristics with the Description of a New Genus and Three New Species

RESEARCH ARTICLE New Insights into Plagiogrammaceae (Bacillariophyta) Based on Multigene Phylogenies and Morphological Characteristics with the Description of a New Genus and Three New Species Chun L. Li1*, Matt P. Ashworth2, Andrzej Witkowski1, Przemysław Dąbek1, Linda K. Medlin3, Wiebe H. C. F. Kooistra4, Shinya Sato5, Izabela Zgłobicka6, Krzysztof J. Kurzydłowski6, Edward C. Theriot7, Jamal S. M. Sabir8, Mohammad A. Khiyami9, Mohammed H. Z. Mutwakil8, Meshaal J. Sabir8, Njud S. Alharbi8, Nahid H. Hajarah8, Song Qing10, Robert K. Jansen2,8 OPEN ACCESS Citation: Li CL, Ashworth MP, Witkowski A, Dąbek P, Medlin LK, Kooistra WHCF, et al. (2015) New Insights into Plagiogrammaceae (Bacillariophyta) Based on Multigene Phylogenies and Morphological Characteristics with the Description of a New Genus and Three New Species. PLoS ONE 10(10): e0139300. doi:10.1371/journal.pone.0139300 Editor: Helge Thorsten Lumbsch, Field Museum of Natural History, UNITED STATES Received: July 10, 2015 Accepted: September 10, 2015 Published: October 14, 2015 Copyright: © 2015 Li et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This research has been funded by Polish National Science Centre (NCN) in Cracow grant no. N2012/04/A/ST10/00544, Grant Recipent AW, available http://www.marinebenthicdiatoms.univ. szczecin.pl/homepage-1. This study also get funded from King Abdulaziz University (KAU) Vice President for Educational Affairs Prof. Dr. Abdulrahman O. Alyoubi and from Chinese Academy of Sciences President’s International Fellowship Initiative (PIFI). 1 Palaeoceanology Unit, Faculty of Geosciences, University of Szczecin, Mickiewicza 18, PL-70-383, Szczecin, Poland, 2 Department of Integrative Biology, University of Texas at Austin, Austin, Texas, United States of America, 3 Marine Biological Association of the UK, The Citadel, Plymouth, United Kingdom PL1 2 PB, 4 Department of Integrative Marine Ecology, Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Napoli, Italy, 5 Faculty of Marine Bioscience, Fukui Prefectural University, Fukui, Japan, 6 Faculty of Materials Science and Engineering, Warsaw University of Technology, Warsaw, Poland, 7 Texas Memorial Museum, University of Texas at Austin, Austin, Texas, United States of America, 8 Biotechnology Research Group, Department of Biological Sciences, Faculty of Science, King Abdulaziz University, Jeddah 21589, Saudi Arabia, 9 King Abdulaziz City for Science and Technology, Riyadh, Saudi Arabia, 10 Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, China * Abstract Plagiogrammaceae, a poorly described family of diatoms, are common inhabitants of the shallow marine littoral zone, occurring either in the sediments or as epiphytes. Previous molecular phylogenies of the Plagiogrammaceae were inferred but included only up to six genera: Plagiogramma, Dimeregramma, Neofragilaria, Talaroneis, Psammogramma and Psammoneis. In this paper, we describe a new plagiogrammoid genus, Orizaformis, obtained from Bohai Sea (China) and present molecular phylogenies of the family based on three and four genes (nuclear-encoded large and small subunit ribosomal RNAs and chloroplast-encoded rbcL and psbC). Also included in the new phylogenies is Glyphodesmis. The phylogenies suggest that the Plagiogrammaceae is composed of two major clades: one consisting of Talaroneis, Orizaformis and Psammoneis, and the second of Glyphodesmis, Psammogramma, Neofragilaria, Dimeregramma and Plagiogramma. In addition, we describe three new species within established genera: Psammoneis obaidii, which was collected from the Red Sea, Saudi Arabia; and Neofragilaria stilus and Talaroneis biacutifrons from the Mozambique Channel, Indian Ocean, and illustrate two new combination taxa: Neofragilaria anomala and Neofragilaria lineata. Our observations suggest that the PLOS ONE | DOI:10.1371/journal.pone.0139300 October 14, 2015 1 / 26 Phylogeny and Morphology of Plagiogrammaceae (Bacillariophyta) The funder has no contributions to study design, data collection and preparation of the manuscript. biodiversity of the family is strongly needed to be researched, and the phylogenetic analyses provide a useful framework for future studies of Plagiogrammaceae. Competing Interests: The authors have declared that no competing interests exist. Introduction The araphid diatom family Plagiogrammaceae was established by De Toni in 1890, and was often confused with other small araphid diatoms because of its broadly defined characters. Seven genera are currently included in the family: Plagiogramma Greville, Dimeregramma Ralfs, Glyphodesmis Greville, Neofragilaria Desikachary, Prasad & Prema, Psammogramma Sato & Medlin, Psammoneis Sato, Kooistra & Medlin and Talaroneis Kooistra & De Stefano, which was proposed to replace the invalidly published Dimeregrammopsis Ricard. A recently proposed circumscription of this family by Sato et al. [1] defined the group thus: (1) elongated valves with parallel striae, oriented perpendicular to the apical axis; (2) a visible sternum in most genera; (3) apical pore fields on valves; (4) absence of rimoportula; and (5) presence of occluded areolae. However, these morphological characteristics of Plagiogrammaceae are not unique among diatoms. Many araphid diatoms have parallel striae and a distinct sternum; many araphid diatoms (and even some centric diatoms, particularly in the Biddulphiaceae and Eupodiscaceae) have apical pore fields; other small araphid pennates (such as Staurosira species) and centrics (Corethron and Leptocylindrus) lack rimoportula; and occluded pores are found in most diatoms, albeit in a variety of siliceous structures. Additionally, these characters are not universally shared by all genera within the Plagiogrammaceae. Psammoneis is the only plagiogrammoid genus in which siliceous areolae occlusions have not been observed thus far, only occasionally remnants of areolar occlusion have been observed [1]. Also, little is known about the biology of these taxa. All we know about their ecology is that they are abundant in the marine littoral zone [1–3]. Perhaps because of morphological ambiguity, the taxonomic position of the Plagiogrammaceae has been controversial. Initially, the family was placed in the araphid diatoms [2,4,5] due to a distinct sternum and a valve outline typical for pennate diatoms. Round & Crawford [6] later transferred Plagiogrammaceae into the subclass Biddulphiophycidae Round & Crawford, the order Triceratiales Round & Crawford, and the family Triceratiaceae. The reason for this was not clearly stated but was likely related to the presence of elaborate apical pore fields resembling ocelli (...truncated)