Consumption of oxygen by astaxanthin biosynthesis

A protective mechanism against oxidative stress in Haematococcus pluvialis (Chlorophyceae)

Yantao Li, Milton Sommerfeld, Feng Chen, Qiang Hu

Research output: Contribution to journalArticle

91 Citations (Scopus)

Abstract

Haematococcus pluvialis, a unicellular green microalga, experiences photooxidative stress when exposed to excess photon flux density (PFD) relative to the capacity of photosynthesis, and particularly under other adverse environmental conditions (e.g., nutrient depletion, salinity, and excess heavy metals). Under stress, Haematococcus cells synthesize and accumulate large amounts of the secondary carotenoid astaxanthin stored in cytosolic lipid bodies. In this study, the transcriptional expression of five astaxanthin biosynthesis genes and two plastid terminal oxidase (PTOX) genes either in high PFD or in the presence of excessive sodium acetate and/or iron was determined by real-time reverse transcription PCR, and astaxanthin accumulation was measured by HPLC. Photosynthetic oxygen evolution, lipid peroxidation, and cell mortality were also investigated under these stress conditions. Our results indicate that the astaxanthin biosynthesis pathway may consume as much as 9.94% of the molecular oxygen evolved from photosynthesis under stress via at least two distinct routes: (1) extensive oxygen-dependent processes leading to astaxanthin formation, and (2) conversion of molecular oxygen into water using electrons derived from carotenogenic desaturation steps to PTOX via the photosynthetic plastoquinone (PQ) pool. Reduction of reactive oxygen species (ROS) production by reducing subcellular molecular oxygen substrates through the astaxanthin biosynthesis pathway may represent a novel protective mechanism to cope with oxidative stress. Reoxidation of the PQ pool by PTOX may further reduce photosynthetic electron transport chain-induced ROS formation.

Original languageEnglish (US)
Pages (from-to)1783-1797
Number of pages15
JournalJournal of Plant Physiology
Volume165
Issue number17
DOIs
StatePublished - Nov 28 2008

Fingerprint

Haematococcus pluvialis
astaxanthin
Chlorophyceae
Oxygen Consumption
oxygen consumption
Oxidative Stress
oxidative stress
biosynthesis
Plastids
Oxygen
Plastoquinone
plastids
oxygen
Oxidoreductases
Photosynthesis
Photons
reactive oxygen species
Reactive Oxygen Species
Haematococcus
photosynthesis

Keywords

  • Astaxanthin
  • Carotenogenesis
  • Haematococcus pluvialis
  • MRNA expression
  • Oxidative stress

ASJC Scopus subject areas

  • Plant Science
  • Physiology
  • Agronomy and Crop Science

Cite this

Consumption of oxygen by astaxanthin biosynthesis : A protective mechanism against oxidative stress in Haematococcus pluvialis (Chlorophyceae). / Li, Yantao; Sommerfeld, Milton; Chen, Feng; Hu, Qiang.

In: Journal of Plant Physiology, Vol. 165, No. 17, 28.11.2008, p. 1783-1797.

Research output: Contribution to journalArticle

@article{129489dd2e274a38b721ad9b858d3221,
title = "Consumption of oxygen by astaxanthin biosynthesis: A protective mechanism against oxidative stress in Haematococcus pluvialis (Chlorophyceae)",
abstract = "Haematococcus pluvialis, a unicellular green microalga, experiences photooxidative stress when exposed to excess photon flux density (PFD) relative to the capacity of photosynthesis, and particularly under other adverse environmental conditions (e.g., nutrient depletion, salinity, and excess heavy metals). Under stress, Haematococcus cells synthesize and accumulate large amounts of the secondary carotenoid astaxanthin stored in cytosolic lipid bodies. In this study, the transcriptional expression of five astaxanthin biosynthesis genes and two plastid terminal oxidase (PTOX) genes either in high PFD or in the presence of excessive sodium acetate and/or iron was determined by real-time reverse transcription PCR, and astaxanthin accumulation was measured by HPLC. Photosynthetic oxygen evolution, lipid peroxidation, and cell mortality were also investigated under these stress conditions. Our results indicate that the astaxanthin biosynthesis pathway may consume as much as 9.94{\%} of the molecular oxygen evolved from photosynthesis under stress via at least two distinct routes: (1) extensive oxygen-dependent processes leading to astaxanthin formation, and (2) conversion of molecular oxygen into water using electrons derived from carotenogenic desaturation steps to PTOX via the photosynthetic plastoquinone (PQ) pool. Reduction of reactive oxygen species (ROS) production by reducing subcellular molecular oxygen substrates through the astaxanthin biosynthesis pathway may represent a novel protective mechanism to cope with oxidative stress. Reoxidation of the PQ pool by PTOX may further reduce photosynthetic electron transport chain-induced ROS formation.",
keywords = "Astaxanthin, Carotenogenesis, Haematococcus pluvialis, MRNA expression, Oxidative stress",
author = "Yantao Li and Milton Sommerfeld and Feng Chen and Qiang Hu",
year = "2008",
month = "11",
day = "28",
doi = "10.1016/j.jplph.2007.12.007",
language = "English (US)",
volume = "165",
pages = "1783--1797",
journal = "Journal of Plant Physiology",
issn = "0176-1617",
publisher = "Urban und Fischer Verlag GmbH und Co. KG",
number = "17",

}

TY - JOUR

T1 - Consumption of oxygen by astaxanthin biosynthesis

T2 - A protective mechanism against oxidative stress in Haematococcus pluvialis (Chlorophyceae)

AU - Li, Yantao

AU - Sommerfeld, Milton

AU - Chen, Feng

AU - Hu, Qiang

PY - 2008/11/28

Y1 - 2008/11/28

N2 - Haematococcus pluvialis, a unicellular green microalga, experiences photooxidative stress when exposed to excess photon flux density (PFD) relative to the capacity of photosynthesis, and particularly under other adverse environmental conditions (e.g., nutrient depletion, salinity, and excess heavy metals). Under stress, Haematococcus cells synthesize and accumulate large amounts of the secondary carotenoid astaxanthin stored in cytosolic lipid bodies. In this study, the transcriptional expression of five astaxanthin biosynthesis genes and two plastid terminal oxidase (PTOX) genes either in high PFD or in the presence of excessive sodium acetate and/or iron was determined by real-time reverse transcription PCR, and astaxanthin accumulation was measured by HPLC. Photosynthetic oxygen evolution, lipid peroxidation, and cell mortality were also investigated under these stress conditions. Our results indicate that the astaxanthin biosynthesis pathway may consume as much as 9.94% of the molecular oxygen evolved from photosynthesis under stress via at least two distinct routes: (1) extensive oxygen-dependent processes leading to astaxanthin formation, and (2) conversion of molecular oxygen into water using electrons derived from carotenogenic desaturation steps to PTOX via the photosynthetic plastoquinone (PQ) pool. Reduction of reactive oxygen species (ROS) production by reducing subcellular molecular oxygen substrates through the astaxanthin biosynthesis pathway may represent a novel protective mechanism to cope with oxidative stress. Reoxidation of the PQ pool by PTOX may further reduce photosynthetic electron transport chain-induced ROS formation.

AB - Haematococcus pluvialis, a unicellular green microalga, experiences photooxidative stress when exposed to excess photon flux density (PFD) relative to the capacity of photosynthesis, and particularly under other adverse environmental conditions (e.g., nutrient depletion, salinity, and excess heavy metals). Under stress, Haematococcus cells synthesize and accumulate large amounts of the secondary carotenoid astaxanthin stored in cytosolic lipid bodies. In this study, the transcriptional expression of five astaxanthin biosynthesis genes and two plastid terminal oxidase (PTOX) genes either in high PFD or in the presence of excessive sodium acetate and/or iron was determined by real-time reverse transcription PCR, and astaxanthin accumulation was measured by HPLC. Photosynthetic oxygen evolution, lipid peroxidation, and cell mortality were also investigated under these stress conditions. Our results indicate that the astaxanthin biosynthesis pathway may consume as much as 9.94% of the molecular oxygen evolved from photosynthesis under stress via at least two distinct routes: (1) extensive oxygen-dependent processes leading to astaxanthin formation, and (2) conversion of molecular oxygen into water using electrons derived from carotenogenic desaturation steps to PTOX via the photosynthetic plastoquinone (PQ) pool. Reduction of reactive oxygen species (ROS) production by reducing subcellular molecular oxygen substrates through the astaxanthin biosynthesis pathway may represent a novel protective mechanism to cope with oxidative stress. Reoxidation of the PQ pool by PTOX may further reduce photosynthetic electron transport chain-induced ROS formation.

KW - Astaxanthin

KW - Carotenogenesis

KW - Haematococcus pluvialis

KW - MRNA expression

KW - Oxidative stress

UR - http://www.scopus.com/inward/record.url?scp=51349091665&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=51349091665&partnerID=8YFLogxK

U2 - 10.1016/j.jplph.2007.12.007

DO - 10.1016/j.jplph.2007.12.007

M3 - Article

VL - 165

SP - 1783

EP - 1797

JO - Journal of Plant Physiology

JF - Journal of Plant Physiology

SN - 0176-1617

IS - 17

ER -