Molecular and physiological evidence of genetic assimilation to high CO2 in the marine nitrogen fixer Trichodesmium.
Most investigations of biogeochemically important microbes have focused on plastic (short-term) phenotypic responses in the absence of genetic change, whereas few have investigated adaptive (long-term) responses. However, no studies to date have investigated the molecular progression underlying the transition from plasticity to adaptation under elevated CO2for a marine nitrogen-fixer. To address this gap, we cultured the globally important cyanobacterium Trichodesmium at both low and high CO2for 4.5 y, followed by reciprocal transplantation experiments to test for adaptation. Intriguingly, fitness actually increased in all high-CO2adapted cell lines in the ancestral environment upon reciprocal transplantation. By leveraging coordinated phenotypic and transcriptomic profiles, we identified expression changes and pathway enrichments that rapidly responded to elevated CO2and were maintained upon adaptation, providing strong evidence for genetic assimilation. These candidate genes and pathways included those involved in photosystems, transcriptional regulation, cell signaling, carbon/nitrogen storage, and energy metabolism. Conversely, significant changes in specific sigma factor expression were only observed upon adaptation. These data reveal genetic assimilation as a potentially adaptive response of Trichodesmium and importantly elucidate underlying metabolic pathways paralleling the fixation of the plastic phenotype upon adaptation, thereby contributing to the few available data demonstrating genetic assimilation in microbial photoautotrophs. These molecular insights are thus critical for identifying pathways under selection as drivers in plasticity and adaptation.
Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089.
Nathan G
NG
Walworth
Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089.
Michael D
MD
Lee
Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089.
Fei-Xue
FX
Fu
Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089.
David A
DA
Hutchins
Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089 eawebb@usc.edu.
Eric A
EA
Webb
D000222:Adaptation, Physiological; D001426:Bacterial Proteins / Q000235:genetics*; D002245:Carbon Dioxide / Q000378:metabolism*; D004734:Energy Metabolism; D020869:Gene Expression Profiling / Q000379:methods; D015964:Gene Expression Regulation, Bacterial; D056084:Genetic Fitness; D009584:Nitrogen / Q000378:metabolism*; D009586:Nitrogen Fixation; D012808:Sigma Factor / Q000235:genetics; D000072359:Trichodesmium / Q000235:genetics / Q000254:growth & development*
D001426:Bacterial Proteins; D012808:Sigma Factor; D002245:Carbon Dioxide; D009584:Nitrogen
CO2; diazotroph; evolution; genetic assimilation; plasticity