Mucus-Trap-Assisted Feeding Is a Common Strategy of the Small Mixoplanktonic <i>Prorocentrum pervagatum</i> and <i>P. cordatum</i> (Prorocentrales, Dinophyceae)

<i>Prorocentrum</i> comprises a diverse group of bloom-forming dinophytes with a worldwide distribution. Although photosynthetic, mixoplanktonic phagotrophy has also been described. Recently, the small <i>P.</i> cf. <i>balticum</i> was shown to use a remarkable fe...

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Main Authors: Urban Tillmann, Aditee Mitra, Kevin J. Flynn, Michaela E. Larsson
Format: Article
Language:English
Published: MDPI AG 2023-07-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/11/7/1730
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author Urban Tillmann
Aditee Mitra
Kevin J. Flynn
Michaela E. Larsson
author_facet Urban Tillmann
Aditee Mitra
Kevin J. Flynn
Michaela E. Larsson
author_sort Urban Tillmann
collection DOAJ
description <i>Prorocentrum</i> comprises a diverse group of bloom-forming dinophytes with a worldwide distribution. Although photosynthetic, mixoplanktonic phagotrophy has also been described. Recently, the small <i>P.</i> cf. <i>balticum</i> was shown to use a remarkable feeding strategy by crafting globular mucus traps to capture and immobilize potential prey. Here we present evidence showing that two additional related species, the recently described <i>P. pervagatum</i> and the cosmopolitan bloom-forming <i>P. cordatum</i>, also produce large (80–120 µm) mucus traps supporting their mixoplanktonic activity. Prey are captured within the traps either through passive entanglement upon contact with the outside surface, or through active water movement created by rotating <i>Prorocentrum</i> cells eddying particles to the inside surface where trapped live prey cells became immobilized. Entrapment in mucus assisted deployment into the prey of a peduncle extruded from the apical area of the <i>Prorocentrum</i> cell. Phagotrophy by <i>P. pervagatum</i> supported faster growth compared to unfed controls and time series quantification of food vacuoles revealed ingestion rates of ca. 10–12 <i>Teleaulax</i> prey cells day<sup>−1</sup>. Model calculations show clear advantages of deploying a mucus trap for increasing prey encounter rates. This study demonstrates that the large size and immobilization properties of mucus traps successfully increase the availability of prey for small <i>Prorocentrum</i> species, whose peduncle feeding mode impedes consumption of actively moving prey, and that this strategy is common among certain clades of small planktonic <i>Prorocentrum</i> species.
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spelling doaj.art-5a739405c2db448498b48c18e75b0b032023-11-18T20:35:39ZengMDPI AGMicroorganisms2076-26072023-07-01117173010.3390/microorganisms11071730Mucus-Trap-Assisted Feeding Is a Common Strategy of the Small Mixoplanktonic <i>Prorocentrum pervagatum</i> and <i>P. cordatum</i> (Prorocentrales, Dinophyceae)Urban Tillmann0Aditee Mitra1Kevin J. Flynn2Michaela E. Larsson3Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, GermanySchool of Earth and Environmental Sciences, Cardiff University, Park Place, Cardiff CF10 3AT, UKPlymouth Marine Laboratory, Plymouth PL1 3DH, UKAquatic Science Branch, Department of Water and Environmental Regulation, Joondalup, WA 6027, Australia<i>Prorocentrum</i> comprises a diverse group of bloom-forming dinophytes with a worldwide distribution. Although photosynthetic, mixoplanktonic phagotrophy has also been described. Recently, the small <i>P.</i> cf. <i>balticum</i> was shown to use a remarkable feeding strategy by crafting globular mucus traps to capture and immobilize potential prey. Here we present evidence showing that two additional related species, the recently described <i>P. pervagatum</i> and the cosmopolitan bloom-forming <i>P. cordatum</i>, also produce large (80–120 µm) mucus traps supporting their mixoplanktonic activity. Prey are captured within the traps either through passive entanglement upon contact with the outside surface, or through active water movement created by rotating <i>Prorocentrum</i> cells eddying particles to the inside surface where trapped live prey cells became immobilized. Entrapment in mucus assisted deployment into the prey of a peduncle extruded from the apical area of the <i>Prorocentrum</i> cell. Phagotrophy by <i>P. pervagatum</i> supported faster growth compared to unfed controls and time series quantification of food vacuoles revealed ingestion rates of ca. 10–12 <i>Teleaulax</i> prey cells day<sup>−1</sup>. Model calculations show clear advantages of deploying a mucus trap for increasing prey encounter rates. This study demonstrates that the large size and immobilization properties of mucus traps successfully increase the availability of prey for small <i>Prorocentrum</i> species, whose peduncle feeding mode impedes consumption of actively moving prey, and that this strategy is common among certain clades of small planktonic <i>Prorocentrum</i> species.https://www.mdpi.com/2076-2607/11/7/1730microalgaemixotrophymixoplanktonpeduncle feedingvideo microscopymodelling
spellingShingle Urban Tillmann
Aditee Mitra
Kevin J. Flynn
Michaela E. Larsson
Mucus-Trap-Assisted Feeding Is a Common Strategy of the Small Mixoplanktonic <i>Prorocentrum pervagatum</i> and <i>P. cordatum</i> (Prorocentrales, Dinophyceae)
Microorganisms
microalgae
mixotrophy
mixoplankton
peduncle feeding
video microscopy
modelling
title Mucus-Trap-Assisted Feeding Is a Common Strategy of the Small Mixoplanktonic <i>Prorocentrum pervagatum</i> and <i>P. cordatum</i> (Prorocentrales, Dinophyceae)
title_full Mucus-Trap-Assisted Feeding Is a Common Strategy of the Small Mixoplanktonic <i>Prorocentrum pervagatum</i> and <i>P. cordatum</i> (Prorocentrales, Dinophyceae)
title_fullStr Mucus-Trap-Assisted Feeding Is a Common Strategy of the Small Mixoplanktonic <i>Prorocentrum pervagatum</i> and <i>P. cordatum</i> (Prorocentrales, Dinophyceae)
title_full_unstemmed Mucus-Trap-Assisted Feeding Is a Common Strategy of the Small Mixoplanktonic <i>Prorocentrum pervagatum</i> and <i>P. cordatum</i> (Prorocentrales, Dinophyceae)
title_short Mucus-Trap-Assisted Feeding Is a Common Strategy of the Small Mixoplanktonic <i>Prorocentrum pervagatum</i> and <i>P. cordatum</i> (Prorocentrales, Dinophyceae)
title_sort mucus trap assisted feeding is a common strategy of the small mixoplanktonic i prorocentrum pervagatum i and i p cordatum i prorocentrales dinophyceae
topic microalgae
mixotrophy
mixoplankton
peduncle feeding
video microscopy
modelling
url https://www.mdpi.com/2076-2607/11/7/1730
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