New observations on the large hemidiscoid diatom Palmerina ostenfeldii and its symbiotic ciliate Vaginicola collariforma sp. nov. from subtropical Australian waters

Abstract

The large hemi-discoid diatom Palmerina ostenfeldii was common in subtropical Moreton Bay, Australia, following a flood in January 2011. All diatom cells exhibited diagnostic subapical folds settled by loricate peritrich ciliates, but which readily abandoned stressed diatom cells. We characterized both diatoms and ciliates by morphological and molecular analyses, including careful video observations on non-preserved cells immediately after collection. The fold in the diatom cell wall comprises a narrow shelf upon which the ciliates attach (on average seven per fold, and similar for the two folds of a single diatom cell) but without penetrating the diatom wall itself. Folds were fully developed in newly formed internal valves, indicating that the ciliates play no role in their morphogenesis. SSU rRNA sequences of P. ostenfeldii from Moreton Bay (with ciliates) differed by 25 bp (1.5%) from those of P. hardmaniana from Texas (without ciliates), but surprisingly rbcL chloroplast sequences for both diatom species were indistinguishable. The ciliate species epiphytic on P. ostenfeldii, previously referred to as the cold-water tintinnid Amphorella borealis could not be assigned to any known species. We formally describe it here as Vaginicola collariforma sp. nov. within the crown clade of peritrichs which also includes the closely related genus Cothurnia (but distinguished as having an external stalk). Beating of the peritrich oral cilia was observed to drive rotational movement of the large discoid diatoms as in a ferris wheel. The observed diatom-ciliate symbiosis may represent a unique evolutionary adaptation in which the ciliate is host-specific and attaches in a specific locality on the host cell.

Keywords:

• Diatom-Ciliate symbioses
• peritrich ciliates
• morphological and molecular analyses
• tropical marine phytoplankton

Supplemental

Supplemental data for this article can be accessed https://doi.org/10.1080/0269249X.2021.1914737

Acknowledgements

We dedicate this paper to the late Prof. John C. Clamp from North Carolina Central University, who worked with us on the Vaginicola species description, until he passed away in February 2018. We also acknowledge the mentorship provided to the first author by esteemed Colombian phytoplanktologist the late Prof. Luis Alfonso Vidal Velásquez. We thank Phillip Ford, Gary Fry, Felipe Gusmao and Kadija Oubelkheir from the CSIRO Wealth from Oceans ORCA theme for collection of samples and environmental information in the Moreton Bay Marine Park after the Brisbane Floods 2011. We thank Frank Coman, Mark Tonks and Claire Davis from CSIRO – Oceans and Atmosphere, and John Ferris, Jacob Gruythuysen, Keryn Reeves, Myles Waller, Darren Renouf, James Fels, Mark Davidson and Joel Hodge from the Department of Environment and Science (Queensland) for collection of fresh samples to isolate living diatoms and ciliates, and Alyssa Budd for assisting with DNA extraction, purification and sequencing of the first batch of Palmerina and Vaginicola. This work was part of an ARC Linkage Grant on the Resilience of Moreton Bay LP0883663 and supported by the Integrated Marine Observing System (IMOS), which is funded by the Australian Government through the National Collaborative Research Infrastructure Strategy and the Super Science Initiative.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This work was supported by Australian Research Council: [Grant Number LP0883663]; Australian Government: [Grant Number IMOS].