Sexual reproduction and auxospore development in the diatom Biddulphia biddulphiana

• Published in: PloS one Vol. 17; no. 9; p. e0272778
• Main Authors: Kaczmarska, Irena, Ehrman, James M, Ashworth, Matt P
• Format: Journal Article
• Language: English
• Published: San Francisco Public Library of Science 06.09.2022; Public Library of Science (PLoS)
• Subjects: Acids; Auxospores; Banded structure; Biddulphia biddulphiana; Biology and Life Sciences; Chloroplasts; Cloning; Complexity; Data search; Developmental stages; Diatoms; Earth Sciences; Fine structure; Identification and classification; Light; Marine microorganisms; Morphology; Organelles; Phylogenetics; Phylogeny; Physiological aspects; Pore size; Reproduction; Reproduction (biology); Research and Analysis Methods; Scanning electron microscopy; Sexual reproduction; Spermatogenesis; Spores (Botany); Stainless steel; Taxonomy; Ultrastructure; Valves; Washers & dryers; Canada; United States > US
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0272778

Phylogenetic relationships among mediophycean diatoms with elliptical valve outline and elevated apices have long been a subject of interest and debate, particularly with respect to their relationship to pennates. However, results remain inconclusive, whether based on vegetative valve morphology, reproduction, or molecular phylogenetic data. Searching for phylogenetically informative features, we re-examined sexual reproduction, auxospore structure and development in the diatom Biddulphia biddulphiana. Several unique or unusual features and processes characterized its sexual reproduction. A unique spermatogenesis occurs with premeiotic separation of an anucleate protoplast containing all chloroplasts and likely other organelles. Additionally, their auxospore walls are some of the most complex documented, retaining earlier deposited layers that obscure layers formed during later stages of development. The oldest layer consists of thick, mostly organic incunabulum, underlain by outer and inner epizonia and finally transverse (TP) and longitudinal (LP) perizonia. The complexity of the fine structure of these layers is unprecedented. The orientation of some TP bands is also unique in mediophytes, with some perpendicular to the auxospore apical axis, parallel to each other, and open with aligned ends, as typically seen in pennates. The TP also contains rings slanting toward the apices, as in some other mediophytes, e.g., eupodiscaceans. However, both eupodiscaceans and biddulphiaceans show perizonial band structure derived from anastomosing radial scales, thus termed "scaly bands". Pinnate TP bands, common among pennate auxospores, were not found. Thus B. biddulphiana auxospore wall structure contains a mixture of characters specific to this clone but also known from mediophytes and araphid pennates. However, these features do not provide unequivocal evidence that this or the other Biddulphia species examined to date are the closest extant relatives of basal araphid pennates.