Metabolic Flexibility Underpins Growth Capabilities of the Fastest Growing Alga

Haim Treves, Omer Murik, Isaac Kedem, Doron Eisenstadt, Sagit Meir, Ilana Rogachev, Jedrzej Szymanski, Nir Keren, Isabel Orf, Antonio F. Tiburcio, Rubén Alcázar, Asaph Aharoni, Joachim Kopka, Aaron Kaplan*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

27 Scopus citations

Abstract

The factors rate-limiting growth of photosynthetic organisms under optimal conditions are controversial [1–8]. Adaptation to extreme environments is usually accompanied by reduced performance under optimal conditions [9, 10]. However, the green alga Chlorella ohadii, isolated from a harsh desert biological soil crust [11–17], does not obey this rule. In addition to resistance to photodamage [17, 18], it performs the fastest growth ever reported for photosynthetic eukaryotes. A multiphasic growth pattern (very fast growth [phase I], followed by growth retardation [phase II] and additional fast growth [phase III]) observed under constant illumination and temperature indicates synchronization of the algal population. Large physiological changes at transitions between growth phases suggest metabolic shifts. Indeed, metabolome analyses at points along the growth phases revealed large changes in the levels of many metabolites during growth with an overall rise during phase I and decline in phase II. Multivariate analysis of the metabolome data highlighted growth phase as the main factor contributing to observed metabolite variance. The analyses identified putrescine as the strongest predictive metabolite for growth phase and a putative growth regulator. Indeed, extracellular additions of polyamines strongly affected the growth rate in phase I and the growth arrest in phase II, with a marked effect on O2 exchange. Our data implicate polyamines as the signals harmonizing metabolic shifts and suggest that metabolic flexibility enables the immense growth capabilities of C. ohadii. The data provide a new dimension to current models focusing on growth-limiting processes in photosynthetic organisms where the anabolic and catabolic metabolisms must be strictly regulated.

Original languageAmerican English
Pages (from-to)2559-2567.e3
JournalCurrent Biology
Volume27
Issue number16
DOIs
StatePublished - 21 Aug 2017

Bibliographical note

Publisher Copyright:
© 2017 Elsevier Ltd

Keywords

  • algae
  • chlorella
  • desert
  • growth
  • metabolome
  • photosynthesis
  • polyamine
  • soil crust

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