Proteomics analysis reveals differential acclimation of coastal and oceanic Synechococcus to climate warming and iron limitation

Cara Schiksnis; Min Xu; Mak A Saito; Matthew McIlvin; Dawn Moran; Xiaopeng Bian; Seth G John; Qiang Zheng; Nina Yang; Feixue Fu; David A Hutchins

doi:10.3389/fmicb.2024.1323499

Proteomics analysis reveals differential acclimation of coastal and oceanic Synechococcus to climate warming and iron limitation

Front Microbiol. 2024 Feb 20:15:1323499. doi: 10.3389/fmicb.2024.1323499. eCollection 2024.

Authors

Cara Schiksnis¹, Min Xu², Mak A Saito³, Matthew McIlvin³, Dawn Moran³, Xiaopeng Bian¹, Seth G John¹, Qiang Zheng⁴, Nina Yang^{1

5

6}, Feixue Fu¹, David A Hutchins¹

Affiliations

¹ Marine and Environmental Biology, University of Southern California, Los Angeles, CA, United States.
² State Key Laboratory of Marine Resource Utilization in South China Sea, Hainan University, Haikou, China.
³ Marine Chemistry and Geochemistry Department, Woods Hole Oceanographic Institution, Woods Hole, MA, United States.
⁴ State Key Laboratory of Marine Environmental Science, Institute of Marine Microbes and Ecospheres, Xiamen University, Xiamen, China.
⁵ Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, United States.
⁶ Marine Policy Center, Woods Hole Oceanographic Institution, Woods Hole, MA, United States.

Abstract

In many oceanic regions, anthropogenic warming will coincide with iron (Fe) limitation. Interactive effects between warming and Fe limitation on phytoplankton physiology and biochemical function are likely, as temperature and Fe availability affect many of the same essential cellular pathways. However, we lack a clear understanding of how globally significant phytoplankton such as the picocyanobacteria Synechococcus will respond to these co-occurring stressors, and what underlying molecular mechanisms will drive this response. Moreover, ecotype-specific adaptations can lead to nuanced differences in responses between strains. In this study, Synechococcus isolates YX04-1 (oceanic) and XM-24 (coastal) from the South China Sea were acclimated to Fe limitation at two temperatures, and their physiological and proteomic responses were compared. Both strains exhibited reduced growth due to warming and Fe limitation. However, coastal XM-24 maintained relatively higher growth rates in response to warming under replete Fe, while its growth was notably more compromised under Fe limitation at both temperatures compared with YX04-1. In response to concurrent heat and Fe stress, oceanic YX04-1 was better able to adjust its photosynthetic proteins and minimize the generation of reactive oxygen species while reducing proteome Fe demand. Its intricate proteomic response likely enabled oceanic YX04-1 to mitigate some of the negative impact of warming on its growth during Fe limitation. Our study highlights how ecologically-shaped adaptations in Synechococcus strains even from proximate oceanic regions can lead to differing physiological and proteomic responses to these climate stressors.

Keywords: Synechococcus; climate change; interactive effects; iron limitation; ocean warming; proteomics.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was funded by the U.S. National Science Foundation grants OCE 2149837 and OCE 1851222 to DH and FF and OCE 1850719 and OCE 2123055 to MS, by the Simons Foundation Award LI-SIAME 00001532 to SJ, and by the National Natural Science Foundation of China 42188102 to QZ.