“Pomacytosis”—Semi-extracellular phagocytosis of cyanobacteria by the smallest marine algae

The smallest algae, less than 3 μm in diameter, are the most abundant eukaryotes of the World Ocean. Their feeding on planktonic bacteria of similar size is globally important but physically enigmatic. Tiny algal cells tightly packed with the voluminous chloroplasts, nucleus, and mitochondria appear...

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Published in:	PLoS biology Vol. 16; no. 1; p. e2003502
Main Authors:	Kamennaya, Nina A., Kennaway, Gabrielle, Fuchs, Bernhard M., Zubkov, Mikhail V.
Format:	Journal Article
Language:	English
Published:	United States Public Library of Science 05.01.2018 Public Library of Science (PLoS)
Subjects:	Algae Aquatic Organisms - physiology Bacteria Biogeochemistry Biology and Life Sciences Braarudosphaera Cell cycle Cell Membrane Cell Nucleus Cell size Chloroplasts Councils Cyanobacteria Cyanobacteria - metabolism Cyanobacteria - physiology Data collection Earth Sciences Ecology and Environmental Sciences Ecosystems Enzymes Eukaryotes Flow cytometry Funding Internalization Library collections Marine algae Microbiological research Mitochondria Nitrogen Nuclei Nuclei (cytology) Oceanography Phagocytosis Phagocytosis - physiology Physiological aspects Prey Prochlorococcus Prochlorococcus - physiology Research and Analysis Methods Short Reports United Kingdom > UK
ISSN:	1545-7885, 1544-9173, 1545-7885
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Abstract	The smallest algae, less than 3 μm in diameter, are the most abundant eukaryotes of the World Ocean. Their feeding on planktonic bacteria of similar size is globally important but physically enigmatic. Tiny algal cells tightly packed with the voluminous chloroplasts, nucleus, and mitochondria appear to have insufficient organelle-free space for prey internalization. Here, we present the first direct observations of how the 1.3-μm algae, which are only 1.6 times bigger in diameter than their prey, hold individual Prochlorococcus cells in their open hemispheric cytostomes. We explain this semi-extracellular phagocytosis by the cell size limitation of the predatory alga, identified as the Braarudosphaera haptophyte with a nitrogen (N2)-fixing endosymbiont. Because the observed semi-extracellular phagocytosis differs from all other types of protistan phagocytosis, we propose to name it "pomacytosis" (from the Greek πώμα for "plug").
AbstractList	The smallest algae, less than 3 [mu]m in diameter, are the most abundant eukaryotes of the World Ocean. Their feeding on planktonic bacteria of similar size is globally important but physically enigmatic. Tiny algal cells tightly packed with the voluminous chloroplasts, nucleus, and mitochondria appear to have insufficient organelle-free space for prey internalization. Here, we present the first direct observations of how the 1.3-[mu]m algae, which are only 1.6 times bigger in diameter than their prey, hold individual Prochlorococcus cells in their open hemispheric cytostomes. We explain this semi-extracellular phagocytosis by the cell size limitation of the predatory alga, identified as the Braarudosphaera haptophyte with a nitrogen (N.sub.2 )-fixing endosymbiont. Because the observed semi-extracellular phagocytosis differs from all other types of protistan phagocytosis, we propose to name it "pomacytosis" (from the Greek [qi]Ï[mu][alpha] for "plug"). The smallest algae, less than 3 Mm in diameter, are the most abundant eukaryotes of the World Ocean. Their feeding on planktonic bacteria of similar size is globally important but physically enigmatic. Tiny algal cells tightly packed with the voluminous chloroplasts, nucleus, and mitochondria appear to have insufficient organelle-free space for prey internalization. Here, we present the first direct observations of how the 1.3-Mm algae, which are only 1.6 times bigger in diameter than their prey, hold individual Prochlorococcus cells in their open hemispheric cytostomes. We explain this semi-extracellular phagocytosis by the cell size limitation of the predatory alga, identified as the Braarudosphaera haptophyte with a nitrogen (N2)-fixing endosymbiont. Because the observed semi-extracellular phagocytosis differs from all other types of protistan phagocytosis, we propose to name it “pomacytosis” (from the Greek [pi]ώM[alpha] for “plug”). The smallest algae, less than 3 μm in diameter, are the most abundant eukaryotes of the World Ocean. Their feeding on planktonic bacteria of similar size is globally important but physically enigmatic. Tiny algal cells tightly packed with the voluminous chloroplasts, nucleus, and mitochondria appear to have insufficient organelle-free space for prey internalization. Here, we present the first direct observations of how the 1.3-μm algae, which are only 1.6 times bigger in diameter than their prey, hold individual Prochlorococcus cells in their open hemispheric cytostomes. We explain this semi-extracellular phagocytosis by the cell size limitation of the predatory alga, identified as the Braarudosphaera haptophyte with a nitrogen (N2)-fixing endosymbiont. Because the observed semi-extracellular phagocytosis differs from all other types of protistan phagocytosis, we propose to name it "pomacytosis" (from the Greek πώμα for "plug").The smallest algae, less than 3 μm in diameter, are the most abundant eukaryotes of the World Ocean. Their feeding on planktonic bacteria of similar size is globally important but physically enigmatic. Tiny algal cells tightly packed with the voluminous chloroplasts, nucleus, and mitochondria appear to have insufficient organelle-free space for prey internalization. Here, we present the first direct observations of how the 1.3-μm algae, which are only 1.6 times bigger in diameter than their prey, hold individual Prochlorococcus cells in their open hemispheric cytostomes. We explain this semi-extracellular phagocytosis by the cell size limitation of the predatory alga, identified as the Braarudosphaera haptophyte with a nitrogen (N2)-fixing endosymbiont. Because the observed semi-extracellular phagocytosis differs from all other types of protistan phagocytosis, we propose to name it "pomacytosis" (from the Greek πώμα for "plug"). The smallest algae, less than 3 μm in diameter, are the most abundant eukaryotes of the World Ocean. Their feeding on planktonic bacteria of similar size is globally important but physically enigmatic. Tiny algal cells tightly packed with the voluminous chloroplasts, nucleus, and mitochondria appear to have insufficient organelle-free space for prey internalization. Here, we present the first direct observations of how the 1.3-μm algae, which are only 1.6 times bigger in diameter than their prey, hold individual Prochlorococcus cells in their open hemispheric cytostomes. We explain this semi-extracellular phagocytosis by the cell size limitation of the predatory alga, identified as the Braarudosphaera haptophyte with a nitrogen (N2)-fixing endosymbiont. Because the observed semi-extracellular phagocytosis differs from all other types of protistan phagocytosis, we propose to name it "pomacytosis" (from the Greek πώμα for "plug"). The smallest algae, less than 3 μm in diameter, are the most abundant eukaryotes of the World Ocean. Their feeding on planktonic bacteria of similar size is globally important but physically enigmatic. Tiny algal cells tightly packed with the voluminous chloroplasts, nucleus, and mitochondria appear to have insufficient organelle-free space for prey internalization. Here, we present the first direct observations of how the 1.3-μm algae, which are only 1.6 times bigger in diameter than their prey, hold individual Prochlorococcus cells in their open hemispheric cytostomes. We explain this semi-extracellular phagocytosis by the cell size limitation of the predatory alga, identified as the Braarudosphaera haptophyte with a nitrogen (N2)–fixing endosymbiont. Because the observed semi-extracellular phagocytosis differs from all other types of protistan phagocytosis, we propose to name it “pomacytosis” (from the Greek πώμα for “plug”). The global significance of microorganisms is a consequence of their astronomical numbers. This is certainly true for the smallest planktonic algae on earth, which are less than 3 μm in diameter and the most numerous eukaryotic organisms of the oceans. Contrary to the general belief that algae use only sunlight and dissolved mineral nutrients to grow, these microscopic plants consume large numbers of bacteria. Their acting as mini-predators on bacteria of nearly their own size is hard to imagine. A tiny algal cell is cramped with organelles—such as nucleus, mitochondria, chloroplasts—and there is simply no space inside this cell to engulf a large bacterium in the usual manner. To find out how the 1.3-μm–diameter haptophyte algae feed, we studied them using high-resolution electron microscopy. We found that prey handling by the alga differs from all other types of cell feeding. We showed that this alga holds the 0.8-μm–diameter prey in the open cytostome (cell mouth) and that, from among planktonic bacteria, the alga apparently selects a ball-shaped Prochlorococcus (an abundant cyanobacteria responsible for most of global photosynthesis) that tightly fits into the open cytostome like a plug. Instead of full prey digestion, we observed that the alga leaves behind the doughnut-shaped carcass of the prey. We conclude that such unusual feeding, which we call “pomacytosis”, of this tiny predatory alga is caused primarily by the space limitation inside its cell.
Audience	Academic
Author	Zubkov, Mikhail V. Kamennaya, Nina A. Kennaway, Gabrielle Fuchs, Bernhard M.
AuthorAffiliation	1 Ocean Biogeochemistry & Ecosystems Research Group, National Oceanography Centre, Southampton, United Kingdom Princeton University, United States of America 3 Max-Planck Institute for Marine Microbiology, Bremen, Germany 2 Imaging and Analysis Centre, Science Facilities, Natural History Museum, London, United Kingdom
AuthorAffiliation_xml	– name: Princeton University, United States of America – name: 2 Imaging and Analysis Centre, Science Facilities, Natural History Museum, London, United Kingdom – name: 1 Ocean Biogeochemistry & Ecosystems Research Group, National Oceanography Centre, Southampton, United Kingdom – name: 3 Max-Planck Institute for Marine Microbiology, Bremen, Germany
Author_xml	– sequence: 1 givenname: Nina A. surname: Kamennaya fullname: Kamennaya, Nina A. – sequence: 2 givenname: Gabrielle surname: Kennaway fullname: Kennaway, Gabrielle – sequence: 3 givenname: Bernhard M. surname: Fuchs fullname: Fuchs, Bernhard M. – sequence: 4 givenname: Mikhail V. orcidid: 0000-0001-7723-6810 surname: Zubkov fullname: Zubkov, Mikhail V.
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Copyright	COPYRIGHT 2018 Public Library of Science 2018 Public Library of Science. 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: Kamennaya NA, Kennaway G, Fuchs BM, Zubkov MV (2018) “Pomacytosis”-Semi-extracellular phagocytosis of cyanobacteria by the smallest marine algae. PLoS Biol 16(1): e2003502. https://doi.org/10.1371/journal.pbio.2003502 2018 Kamennaya et al 2018 Kamennaya et al 2018 Public Library of Science. 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: Kamennaya NA, Kennaway G, Fuchs BM, Zubkov MV (2018) “Pomacytosis”-Semi-extracellular phagocytosis of cyanobacteria by the smallest marine algae. PLoS Biol 16(1): e2003502. https://doi.org/10.1371/journal.pbio.2003502
Copyright_xml	– notice: COPYRIGHT 2018 Public Library of Science – notice: 2018 Public Library of Science. 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: Kamennaya NA, Kennaway G, Fuchs BM, Zubkov MV (2018) “Pomacytosis”-Semi-extracellular phagocytosis of cyanobacteria by the smallest marine algae. PLoS Biol 16(1): e2003502. https://doi.org/10.1371/journal.pbio.2003502 – notice: 2018 Kamennaya et al 2018 Kamennaya et al – notice: 2018 Public Library of Science. 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: Kamennaya NA, Kennaway G, Fuchs BM, Zubkov MV (2018) “Pomacytosis”-Semi-extracellular phagocytosis of cyanobacteria by the smallest marine algae. PLoS Biol 16(1): e2003502. https://doi.org/10.1371/journal.pbio.2003502
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SubjectTerms	Algae Aquatic Organisms - physiology Bacteria Biogeochemistry Biology and Life Sciences Braarudosphaera Cell cycle Cell Membrane Cell Nucleus Cell size Chloroplasts Councils Cyanobacteria Cyanobacteria - metabolism Cyanobacteria - physiology Data collection Earth Sciences Ecology and Environmental Sciences Ecosystems Enzymes Eukaryotes Flow cytometry Funding Internalization Library collections Marine algae Microbiological research Mitochondria Nitrogen Nuclei Nuclei (cytology) Oceanography Phagocytosis Phagocytosis - physiology Physiological aspects Prey Prochlorococcus Prochlorococcus - physiology Research and Analysis Methods Short Reports
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Title	“Pomacytosis”—Semi-extracellular phagocytosis of cyanobacteria by the smallest marine algae
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