Temporal phosphate gradients reveal diverse acclimation responses in phytoplankton phosphate uptake Carlos

被引:24
作者
Caceres, Carlos [1 ,2 ]
Spatharis, Sofie [3 ,4 ]
Kaiserli, Eirini [5 ]
Smeti, Evangelia [6 ]
Flowers, Hugh [7 ]
Bonachela, Juan A. [1 ,8 ]
机构
[1] Univ Strathclyde, Dept Math & Stat, Livingstone Tower,26 Richmond St, Glasgow G1 1XH, Lanark, Scotland
[2] Ohio State Univ, Sch Environm & Nat Resources, Schiermeier Olentangy River Wetland Res Pk, Columbus, OH 43202 USA
[3] Univ Glasgow, Inst Biodivers Anim Hlth & Comparat Med, Glasgow G12 8QQ, Lanark, Scotland
[4] Univ Glasgow, Sch Life Sci, Glasgow G12 8QQ, Lanark, Scotland
[5] Univ Glasgow, Inst Mol Cell & Syst Biol, Coll Med Vet & Life Sci, Glasgow G12 8QQ, Lanark, Scotland
[6] Hellen Ctr Marine Res, Inst Marine Biol Resources & Inland Waters, 46-7 Km Athens Sounio Ave, Anavyssos 19013, Greece
[7] Univ Glasgow, Dept Chem, Glasgow G12 8QQ, Lanark, Scotland
[8] Rutgers State Univ, Dept Ecol Evolut & Nat Resources, 14 Coll Farm Rd, New Brunswick, NJ 08901 USA
基金
英国生物技术与生命科学研究理事会;
关键词
NUTRIENT-UPTAKE; PHOSPHORUS STARVATION; MARINE-PHYTOPLANKTON; GROWTH-KINETICS; LIMITED GROWTH; NITRATE UPTAKE; SPX DOMAIN; LIMITATION; DIATOM; ECOLOGY;
D O I
10.1038/s41396-019-0473-1
中图分类号
Q14 [生态学(生物生态学)];
学科分类号
071012 ; 0713 ;
摘要
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 (V-max) 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 V-max variations. In addition, our mathematical model reproduced the empirical V-max 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.
引用
收藏
页码:2834 / 2845
页数:12
相关论文
共 57 条
[21]   SLOPE OF THE MONOD EQUATION AS AN INDICATOR OF ADVANTAGE IN NUTRIENT COMPETITION [J].
HEALEY, FP .
MICROBIAL ECOLOGY, 1980, 5 (04) :281-286
[22]   The SPX domain of the yeast low-affinity phosphate transporter Pho90 regulates transport activity [J].
Huerlimann, Hans Caspar ;
Pinson, Benoit ;
Stadler-Waibel, Martha ;
Zeeman, Samuel C. ;
Freimoser, Florian M. .
EMBO REPORTS, 2009, 10 (09) :1003-1008
[23]   Integration of Light and Photoperiodic Signaling in Transcriptional Nuclear Foci [J].
Kaiserli, Eirini ;
Paldi, Katalin ;
O'Donnell, Liz ;
Batalov, Olga ;
Pedmale, Ullas V. ;
Nusinow, Dmitri A. ;
Kay, Steve A. ;
Chory, Joanne .
DEVELOPMENTAL CELL, 2015, 35 (03) :311-321
[24]   A model of flexible uptake of two essential resources [J].
Klausmeier, C. A. ;
Litchman, E. ;
Levin, S. A. .
JOURNAL OF THEORETICAL BIOLOGY, 2007, 246 (02) :278-289
[25]   Effects of phosphorus starvation versus limitation on the marine cyanobacterium Prochlorococcus MED4 I: uptake physiology [J].
Krumhardt, Kristen M. ;
Callnan, Kate ;
Roache-Johnson, Kathryn ;
Swett, Tammy ;
Robinson, Daniela ;
Reistetter, Emily Nahas ;
Saunders, Jaclyn K. ;
Rocap, Gabrielle ;
Moore, Lisa R. .
ENVIRONMENTAL MICROBIOLOGY, 2013, 15 (07) :2114-2128
[26]   Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton [J].
Lin, Senjie ;
Litaker, Richard Wayne ;
Sunda, William G. .
JOURNAL OF PHYCOLOGY, 2016, 52 (01) :10-36
[27]   Trait-Based Community Ecology of Phytoplankton [J].
Litchman, Elena ;
Klausmeier, Christopher A. .
ANNUAL REVIEW OF ECOLOGY EVOLUTION AND SYSTEMATICS, 2008, 39 :615-639
[28]   Changes in gene expression of Prymnesium parvum induced by nitrogen and phosphorus limitation [J].
Liu, Zhenfeng ;
Koid, Amy E. ;
Terrado, Ramon ;
Campbell, Victoria ;
Caron, David A. ;
Heidelberg, Karla B. .
FRONTIERS IN MICROBIOLOGY, 2015, 6
[29]   Impact of ocean phytoplankton diversity on phosphate uptake [J].
Lomas, Michael W. ;
Bonachela, Juan A. ;
Levin, Simon A. ;
Martiny, Adam C. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2014, 111 (49) :17540-17545
[30]  
Mann K.H., 2013, DYNAMICS MARINE ECOS, DOI DOI 10.1007/BF00042919