Auxosporulation in Paralia guyana MacGillivary (Bacillariophyta) and Possible New Insights into the Habit of the Earliest Diatoms

Abstract

BackgroundDiatoms are one of the most ecologically important aquatic micro-eukaryotes. As a group unambiguously recognized as diatoms, they seem to have appeared relatively recently with a limited record of putative remains from oldest sediments. In contrast, molecular clock estimates for the earliest possible emergence of diatoms suggest a considerably older date. Depending on the analysis, Paralia and Leptocylindrus have been recovered within the basal molecular divergences of diatoms. Thus these genera may be in the position to inform on characters that the earliest diatoms possessed.FindingsHere we present auxospore development and structure of initial and post-auxospore cells in a representative of the ancient non-polar centric genus Paralia. Their initial frustules showed unusual, but not unprecedented, spore-like morphology. Similarly, initial frustules of Leptocylindrus have been long considered resting spores and a unique peculiarity of this genus. However, even though spore-like in appearance, initial cells of Paralia readily resumed mitotic divisions. In addition, Paralia post-auxospore cells underwent several rounds of mitoses in a multi-step process of building a typical, “perfect” vegetative valve. This degree of heteromorphy immediately post-auxosporulation is thus far unknown among the diatoms.ImplicationsA spore-related origin of diatoms has already been considered, most recently in the form of the “multiplate diploid cyst” hypothesis. Our discovery that the initial cells in some of the most ancient diatom lineages are structurally spore-like is consistent with that hypothesis because the earliest diatoms may be expected to look somewhat similar to their ancestors. We speculate that because the earliest diatoms may have appeared less diatom-like and more spore-like, they could have gone unrecognized as such in the Triassic/Jurassic sediments. If correct, diatoms may indeed be much older than the fossil record indicates, and possibly more in line with some molecular clock predictions.

Diatom life cycles and ecology in the Cretaceous

“…The likelihood is that they were neritic to coastal (Harwood and Nikolaev , Nikolaev and Harwood , Harwood et al. , Kaczmarska and Ehrman ) at a time when the ocean food chain was very different from today and dominated by planktonic foraminifera, belemnites, ammonites, and marine reptiles. Selection was acting on the cell morphology that would eventually result in adaptations that would permit diatoms to fully colonize the oceans.…”

Ardissonea crystallina has a type of sexual reproduction that is unusual for centric diatoms

“…Divergence between non-polar centric and polar diatoms is strongly suggested by the type and structure of their auxospores (e.g. refs 53 , 54 , except for Thalassiosirales). In radial centrics auxospores expand isometrically; polar centrics and pennates grow anisometrically because of specific auxospore walls containing either only incunabula or incanubula and perizonial bands, respectively.…”

Sexual reproduction in plagiogrammacean diatoms: First insights into the early pennates

“…The interest in applying reproductive characters in phylogenetic studies of araphid diatoms has been slowly growing in the last decade [ 13 , 14 , 31 , 88 ], because sex-related characters are relevant for species survival, and as such they are generally strongly conserved. This is why they are also often used to infer deep divergences in a wide range of organisms [ 89 – 91 ], including diatoms [ 2 , 6 – 8 , 24 , 27 , 92 ].…”

“…Modern research interest in diatom auxospore structure and development began as soon as electron microscopes became commercially available; first using transmission electron microscopy (TEM) in the early 1970s [ 1 , 2 ], and then scanning electron microscopy (SEM) about a decade later [ 3 , 4 ]. This work delivered many unanticipated results, some of which culminated in novel ideas about the origin of diatoms [ 5 , 6 ] and relationships between various lineages within diatoms [ 2 , 7 , 8 ]. Most of that research, however, focused on centrics and raphid pennates.…”