Temporal phosphate gradients reveal diverse acclimation responses in phytoplankton phosphate uptake

Caceres, C., Spatharis, S. , Kaiserli, E. , Smeti, E., Flowers, H. and Bonachela, J. A. (2019) Temporal phosphate gradients reveal diverse acclimation responses in phytoplankton phosphate uptake. ISME Journal, 13(11), pp. 2834-2845. (doi: 10.1038/s41396-019-0473-1) (PMID:31350454)

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Abstract

Phytoplankton face environmental nutrient variations that occur in the dynamic upper layers of the ocean. Phytoplankton cells are able to rapidly acclimate to nutrient fluctuations by adjusting their nutrient-uptake system and metabolism. Disentangling these acclimation responses is a critical step in bridging the gap between phytoplankton cellular physiology and community ecology. Here, we analyzed the dynamics of phosphate (P) uptake acclimation responses along different P temporal gradients by using batch cultures of the diatom Phaeodactylum tricornutum. We employed a multidisciplinary approach that combined nutrient-uptake bioassays, transcriptomic analysis, and mathematical models. Our results indicated that cells increase their maximum nutrient-uptake rate (Vmax) both in response to P pulses and strong phosphorus limitation. The upregulation of three genes coding for different P transporters in cells experiencing low intracellular phosphorus levels supported some of the observed Vmax variations. In addition, our mathematical model reproduced the empirical Vmax patterns by including two types of P transporters upregulated at medium-high environmental and low intracellular phosphorus levels, respectively. Our results highlight the existence of a sequence of acclimation stages along the phosphate continuum that can be understood as a succession of acclimation responses. We provide a novel conceptual framework that can contribute to integrating and understanding the dynamics and wide diversity of acclimation responses developed by phytoplankton.

Item Type:Articles
Additional Information:This research has been supported by the Marine Alliance for Science and Technology for Scotland (MASTS). C.C., S.S., and J.A.B. were supported by the Marine Alliance for Science and Technology for Scotland (MASTS) pooling initiative, funded by the Scottish Funding Council (HR09011) and contributing institutions. Gene expression experiments and analysis performed by E.K. were funded by the Biotechnology and Biological Sciences Research Council (BBSRC) (Grant Award BB/M023079/1).
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Caceres, Dr Carlos and Kaiserli, Dr Eirini and Spatharis, Dr Sofie
Authors: Caceres, C., Spatharis, S., Kaiserli, E., Smeti, E., Flowers, H., and Bonachela, J. A.
College/School:College of Medical Veterinary and Life Sciences > School of Molecular Biosciences
College of Medical Veterinary and Life Sciences > School of Life Sciences
College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
Journal Name:ISME Journal
Publisher:Springer Nature
ISSN:1751-7362
ISSN (Online):1751-7370
Published Online:26 July 2019
Copyright Holders:Copyright © 2019 The Authors
First Published:First published in ISME Journal 13(11):2834-2845
Publisher Policy:Reproduced in accordance with the publisher copyright policy

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
682711Transcriptional regulation of plant growth in nuclear microdomainsEirini KaiserliBiotechnology and Biological Sciences Research Council (BBSRC)BB/M023079/1RI MOLECULAR CELL & SYSTEMS BIOLOGY