TY - JOUR
T1 - Temperature variability interacts with mean temperature to influence the predictability of microbial phenotypes
AU - Fu, Fei Xue
AU - Tschitschko, Bernhard
AU - Hutchins, David A.
AU - Larsson, Michaela E.
AU - Baker, Kirralee G.
AU - McInnes, Allison
AU - Kahlke, Tim
AU - Verma, Arjun
AU - Murray, Shauna A.
AU - Doblin, Martina A.
N1 - Funding Information:
This research was funded by the Australian Government through the Australian Research Council Discovery Scheme (project no. DP140101340 awarded to MD, SM, and DH and DP180100054 awarded to MD). FF and DH were funded by a University of Technology Sydney Distinguished Visiting Professor Scheme. Additional support was provided by U.S. National Science Foundation grant OCE 1638804 to DH and OCE 1851222 to FF and DH. KB, ML were each supported by an Australian Government Training Program Scholarship.
Publisher Copyright:
© 2022 The Authors. Global Change Biology published by John Wiley & Sons Ltd.
PY - 2022/10
Y1 - 2022/10
N2 - Despite their relatively high thermal optima (Topt), tropical taxa may be particularly vulnerable to a rising baseline and increased temperature variation because they live in relatively stable temperatures closer to their Topt. We examined how microbial eukaryotes with differing thermal histories responded to temperature fluctuations of different amplitudes (0 control, ±2, ±4°C) around mean temperatures below or above their Topt. Cosmopolitan dinoflagellates were selected based on their distinct thermal traits and included two species of the same genus (tropical and temperate Coolia spp.), and two strains of the same species maintained at different temperatures for >500 generations (tropical Amphidinium massartii control temperature and high temperature, CT and HT, respectively). There was a universal decline in population growth rate under temperature fluctuations, but strains with narrower thermal niche breadth (temperate Coolia and HT) showed ~10% greater reduction in growth. At suboptimal mean temperatures, cells in the cool phase of the fluctuation stopped dividing, fixed less carbon (C) and had enlarged cell volumes that scaled positively with elemental C, N, and P and C:Chlorophyll-a. However, at a supra-optimal mean temperature, fixed C was directed away from cell division and novel trait combinations developed, leading to greater phenotypic diversity. At the molecular level, heat-shock proteins, and chaperones, in addition to transcripts involving genome rearrangements, were upregulated in CT and HT during the warm phase of the supra-optimal fluctuation (30 ± 4°C), a stress response indicating protection. In contrast, the tropical Coolia species upregulated major energy pathways in the warm phase of its supra-optimal fluctuation (25 ± 4°C), indicating a broadscale shift in metabolism. Our results demonstrate divergent effects between taxa and that temporal variability in environmental conditions interacts with changes in the thermal mean to mediate microbial responses to global change, with implications for biogeochemical cycling.
AB - Despite their relatively high thermal optima (Topt), tropical taxa may be particularly vulnerable to a rising baseline and increased temperature variation because they live in relatively stable temperatures closer to their Topt. We examined how microbial eukaryotes with differing thermal histories responded to temperature fluctuations of different amplitudes (0 control, ±2, ±4°C) around mean temperatures below or above their Topt. Cosmopolitan dinoflagellates were selected based on their distinct thermal traits and included two species of the same genus (tropical and temperate Coolia spp.), and two strains of the same species maintained at different temperatures for >500 generations (tropical Amphidinium massartii control temperature and high temperature, CT and HT, respectively). There was a universal decline in population growth rate under temperature fluctuations, but strains with narrower thermal niche breadth (temperate Coolia and HT) showed ~10% greater reduction in growth. At suboptimal mean temperatures, cells in the cool phase of the fluctuation stopped dividing, fixed less carbon (C) and had enlarged cell volumes that scaled positively with elemental C, N, and P and C:Chlorophyll-a. However, at a supra-optimal mean temperature, fixed C was directed away from cell division and novel trait combinations developed, leading to greater phenotypic diversity. At the molecular level, heat-shock proteins, and chaperones, in addition to transcripts involving genome rearrangements, were upregulated in CT and HT during the warm phase of the supra-optimal fluctuation (30 ± 4°C), a stress response indicating protection. In contrast, the tropical Coolia species upregulated major energy pathways in the warm phase of its supra-optimal fluctuation (25 ± 4°C), indicating a broadscale shift in metabolism. Our results demonstrate divergent effects between taxa and that temporal variability in environmental conditions interacts with changes in the thermal mean to mediate microbial responses to global change, with implications for biogeochemical cycling.
KW - climate impact
KW - climate variability
KW - dinoflagellate
KW - primary productivity
UR - http://www.scopus.com/inward/record.url?scp=85134477092&partnerID=8YFLogxK
U2 - 10.1111/gcb.16330
DO - 10.1111/gcb.16330
M3 - Article
C2 - 35795906
AN - SCOPUS:85134477092
SN - 1354-1013
VL - 28
SP - 5741
EP - 5754
JO - Global Change Biology
JF - Global Change Biology
IS - 19
ER -