Cell size influences inorganic carbon acquisition in artificially selected phytoplankton

Martino E. Malerba; Dustin J. Marshall; Maria M. Palacios; John A. Raven; John Beardall

doi:10.1111/nph.17068

Cell size influences inorganic carbon acquisition in artificially selected phytoplankton

Martino E. Malerba (Lead / Corresponding author), Dustin J. Marshall, Maria M. Palacios, John A. Raven, John Beardall

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Abstract

· Cell size influences the rate at which phytoplankton assimilate dissolved inorganic carbon (DIC), but it is unclear whether volume-specific carbon uptake should be greater in smaller or larger cells. On the one hand, Fick’s Law predicts smaller cells to have a superior diffusive CO ₂ supply. On the other, larger cells may have greater scope to invest metabolic energy to upregulate active transport per unit area through CO ₂-concentrating mechanisms (CCMs).

· Previous studies have focused on among-species comparisons, which complicates disentangling the role of cell size from other covarying traits. In this study, we investigated the DIC assimilation of the green alga Dunaliella tertiolecta after using artificial selection to evolve a 9.3-fold difference in cell volume. We compared CO ₂ affinity, external carbonic anhydrase (CA _ext), isotopic signatures (δ ¹³C) and growth among size-selected lineages.

· Evolving cells to larger sizes led to an upregulation of CCMs that improved the DIC uptake of this species, with higher CO ₂ affinity, higher CA _ext and higher δ ¹³C. Larger cells also achieved faster growth and higher maximum biovolume densities.

· We showed that evolutionary shifts in cell size can alter the efficiency of DIC uptake systems to influence the fitness of a phytoplankton species.

Original language	English
Pages (from-to)	2647-2659
Number of pages	13
Journal	New Phytologist
Volume	229
Issue number	5
Early online date	6 Nov 2020
DOIs	https://doi.org/10.1111/nph.17068
Publication status	Published - Mar 2021

Keywords

CO2-concentrating mechanisms
carbonic anhydrase
cell size
external carbonic anhydrase
green algae
inorganic carbon
photosynthetic O evolution

ASJC Scopus subject areas

Physiology
Plant Science

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10.1111/nph.17068

Author Accepted ManuscriptAccepted author manuscript, 18.7 MB

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@article{6aa9efdefe6149aebcefea7f0dcfdb62,

title = "Cell size influences inorganic carbon acquisition in artificially selected phytoplankton",

abstract = "· Cell size influences the rate at which phytoplankton assimilate dissolved inorganic carbon (DIC), but it is unclear whether volume-specific carbon uptake should be greater in smaller or larger cells. On the one hand, Fick{\textquoteright}s Law predicts smaller cells to have a superior diffusive CO 2 supply. On the other, larger cells may have greater scope to invest metabolic energy to upregulate active transport per unit area through CO 2-concentrating mechanisms (CCMs).· Previous studies have focused on among-species comparisons, which complicates disentangling the role of cell size from other covarying traits. In this study, we investigated the DIC assimilation of the green alga Dunaliella tertiolecta after using artificial selection to evolve a 9.3-fold difference in cell volume. We compared CO 2 affinity, external carbonic anhydrase (CA ext), isotopic signatures (δ 13C) and growth among size-selected lineages.· Evolving cells to larger sizes led to an upregulation of CCMs that improved the DIC uptake of this species, with higher CO 2 affinity, higher CA ext and higher δ 13C. Larger cells also achieved faster growth and higher maximum biovolume densities.· We showed that evolutionary shifts in cell size can alter the efficiency of DIC uptake systems to influence the fitness of a phytoplankton species. ",

keywords = "CO2-concentrating mechanisms, carbonic anhydrase, cell size, external carbonic anhydrase, green algae, inorganic carbon, photosynthetic O evolution",

author = "Malerba, {Martino E.} and Marshall, {Dustin J.} and Palacios, {Maria M.} and Raven, {John A.} and John Beardall",

note = "Funding Information: We thank Lucy Chapman, Belinda Comerford, Dr Tamsyne Smith‐Harding, Dr Thomas Lines and Dr Yussi Palacios Delgado for their help with laboratory procedures. We also thank the Monash Centre for Electron Microscopy for their help with cell imaging, in particular Dr Georg Ramm, Dr Simon Crawford and Dr Joan Clark. We are grateful to the Water Studies Centre at Monash University for their help with measuring isotopic signatures, especially Prof. Perran Cook and Dr Wei Wen Wong. We would like to express our gratitude to Lesley Wiadrowski, Stewart Crowley and John Arvanitakis for logistical support at Monash University. Finally, we are particularly grateful to the Australian Research Council for financial support. The University of Dundee is a registered Scottish charity (no. 015096). Publisher Copyright: {\textcopyright} 2020 The Authors New Phytologist {\textcopyright} 2020 New Phytologist Foundation",

year = "2021",

month = mar,

doi = "10.1111/nph.17068",

language = "English",

volume = "229",

pages = "2647--2659",

journal = "New Phytologist",

issn = "0028-646X",

publisher = "Wiley-Blackwell",

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T1 - Cell size influences inorganic carbon acquisition in artificially selected phytoplankton

AU - Malerba, Martino E.

AU - Marshall, Dustin J.

AU - Palacios, Maria M.

AU - Raven, John A.

AU - Beardall, John

N1 - Funding Information: We thank Lucy Chapman, Belinda Comerford, Dr Tamsyne Smith‐Harding, Dr Thomas Lines and Dr Yussi Palacios Delgado for their help with laboratory procedures. We also thank the Monash Centre for Electron Microscopy for their help with cell imaging, in particular Dr Georg Ramm, Dr Simon Crawford and Dr Joan Clark. We are grateful to the Water Studies Centre at Monash University for their help with measuring isotopic signatures, especially Prof. Perran Cook and Dr Wei Wen Wong. We would like to express our gratitude to Lesley Wiadrowski, Stewart Crowley and John Arvanitakis for logistical support at Monash University. Finally, we are particularly grateful to the Australian Research Council for financial support. The University of Dundee is a registered Scottish charity (no. 015096). Publisher Copyright: © 2020 The Authors New Phytologist © 2020 New Phytologist Foundation

PY - 2021/3

Y1 - 2021/3

N2 - · Cell size influences the rate at which phytoplankton assimilate dissolved inorganic carbon (DIC), but it is unclear whether volume-specific carbon uptake should be greater in smaller or larger cells. On the one hand, Fick’s Law predicts smaller cells to have a superior diffusive CO 2 supply. On the other, larger cells may have greater scope to invest metabolic energy to upregulate active transport per unit area through CO 2-concentrating mechanisms (CCMs).· Previous studies have focused on among-species comparisons, which complicates disentangling the role of cell size from other covarying traits. In this study, we investigated the DIC assimilation of the green alga Dunaliella tertiolecta after using artificial selection to evolve a 9.3-fold difference in cell volume. We compared CO 2 affinity, external carbonic anhydrase (CA ext), isotopic signatures (δ 13C) and growth among size-selected lineages.· Evolving cells to larger sizes led to an upregulation of CCMs that improved the DIC uptake of this species, with higher CO 2 affinity, higher CA ext and higher δ 13C. Larger cells also achieved faster growth and higher maximum biovolume densities.· We showed that evolutionary shifts in cell size can alter the efficiency of DIC uptake systems to influence the fitness of a phytoplankton species.

AB - · Cell size influences the rate at which phytoplankton assimilate dissolved inorganic carbon (DIC), but it is unclear whether volume-specific carbon uptake should be greater in smaller or larger cells. On the one hand, Fick’s Law predicts smaller cells to have a superior diffusive CO 2 supply. On the other, larger cells may have greater scope to invest metabolic energy to upregulate active transport per unit area through CO 2-concentrating mechanisms (CCMs).· Previous studies have focused on among-species comparisons, which complicates disentangling the role of cell size from other covarying traits. In this study, we investigated the DIC assimilation of the green alga Dunaliella tertiolecta after using artificial selection to evolve a 9.3-fold difference in cell volume. We compared CO 2 affinity, external carbonic anhydrase (CA ext), isotopic signatures (δ 13C) and growth among size-selected lineages.· Evolving cells to larger sizes led to an upregulation of CCMs that improved the DIC uptake of this species, with higher CO 2 affinity, higher CA ext and higher δ 13C. Larger cells also achieved faster growth and higher maximum biovolume densities.· We showed that evolutionary shifts in cell size can alter the efficiency of DIC uptake systems to influence the fitness of a phytoplankton species.

KW - CO2-concentrating mechanisms

KW - carbonic anhydrase

KW - cell size

KW - external carbonic anhydrase

KW - green algae

KW - inorganic carbon

KW - photosynthetic O evolution

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DO - 10.1111/nph.17068

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SN - 0028-646X

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EP - 2659

JO - New Phytologist

JF - New Phytologist

IS - 5

ER -

Cell size influences inorganic carbon acquisition in artificially selected phytoplankton

Abstract

Keywords

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