Temperature variability interacts with mean temperature to influence the predictability of microbial phenotypes

Fei-Xue Fu; Bernhard Tschitschko; David A Hutchins; Michaela E Larsson; Kirralee G Baker; Allison McInnes; Tim Kahlke; Arjun Verma; Shauna A Murray; Martina A Doblin

doi:10.1111/gcb.16330

Temperature variability interacts with mean temperature to influence the predictability of microbial phenotypes

Glob Chang Biol. 2022 Oct;28(19):5741-5754. doi: 10.1111/gcb.16330. Epub 2022 Jul 20.

Authors

Fei-Xue Fu¹, Bernhard Tschitschko^{2

3}, David A Hutchins¹, Michaela E Larsson², Kirralee G Baker^{2

4}, Allison McInnes^{2

5}, Tim Kahlke², Arjun Verma^{2

6}, Shauna A Murray^{2

6

7}, Martina A Doblin^{2

7}

Affiliations

¹ Department of Biological Sciences, University of Southern California, Los Angeles, California, USA.
² Climate Change Cluster, University of Technology Sydney, Ultimo, New South Wales, Australia.
³ Max Planck Institute for Marine Microbiology, Bremen, Germany.
⁴ Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, Australia.
⁵ Centre for Microbiome Research, School of Biomedical Sciences, Translational Research Institute, Queensland University of Technology, Woolloongabba, Queensland, Australia.
⁶ School of Life Sciences, University of Technology Sydney, Ultimo, New South Wales, Australia.
⁷ Sydney Institute of Marine Science, Mosman, New South Wales, Australia.

Abstract

Despite their relatively high thermal optima (T_opt ), tropical taxa may be particularly vulnerable to a rising baseline and increased temperature variation because they live in relatively stable temperatures closer to their T_opt . 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 T_opt . 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.

Keywords: climate impact; climate variability; dinoflagellate; primary productivity.

MeSH terms

Climate Change*
Cold Temperature
Dinoflagellida* / genetics
Hot Temperature
Phenotype
Temperature