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Title: Responses of the picoprasinophyte Micromonas commoda to light and ultraviolet stress

Abstract

Micromonas is a unicellular marine green alga that thrives from tropical to polar ecosystems. We investigated the growth and cellular characteristics of acclimated mid-exponential phase Micromonas commoda RCC299 over multiple light levels and over the diel cycle (14:10 hour light:dark). We also exposed the light:dark acclimated M. commoda to experimental shifts from moderate to high light (HL), and to HL plus ultraviolet radiation (HL+UV), 4.5 hours into the light period. Cellular responses of this prasinophyte were quantified by flow cytometry and changes in gene expression by qPCR and RNA-seq. While proxies for chlorophyll a content and cell size exhibited similar diel variations in HL and controls, with progressive increases during day and decreases at night, both parameters sharply decreased after the HL+UV shift. Two distinct transcriptional responses were observed among chloroplast genes in the light shift experiments: i) expression of transcription and translation-related genes decreased over the time course, and this transition occurred earlier in treatments than controls; ii) expression of several photosystem I and II genes increased in HL relative to controls, as did the growth rate within the same diel period. However, expression of these genes decreased in HL+UV, likely as a photoprotective mechanism. RNA-seq also revealed twomore » genes in the chloroplast genome, ycf2-like and ycf1-like, that had not previously been reported. The latter encodes the second largest chloroplast protein in Micromonas and has weak homology to plant Ycf1, an essential component of the plant protein translocon. Analysis of several nuclear genes showed that the expression of LHCSR2, which is involved in non-photochemical quenching, and five light-harvesting-like genes, increased 30 to >50-fold in HL+UV, but was largely unchanged in HL and controls. Under HL alone, a gene encoding a novel nitrite reductase fusion protein (NIRFU) increased, possibly reflecting enhanced N-assimilation under the 625 μmol photons m -2 s -1 supplied in the HL treatment. NIRFU's domain structure suggests it may have more efficient electron transfer than plant NIR proteins. Lastly, our analyses indicate that Micromonas can readily respond to abrupt environmental changes, such that strong photoinhibition was provoked by combined exposure to HL and UV, but a ca. 6-fold increase in light was stimulatory.« less

Authors:
 [1];  [1];  [1];  [1];  [2];  [3]; ORCiD logo [4]
  1. Monterey Bay Aquarium Research Inst. (MBARI), Moss Landing, CA (United States)
  2. Univ. of California, Santa Cruz, CA (United States). Dept. of Biomolecular Engineering
  3. Sorbonne Univ., Roscoff (France). Station Biologique
  4. Monterey Bay Aquarium Research Inst. (MBARI), Moss Landing, CA (United States); Univ. of California, Santa Cruz, CA (United States). Dept. of Ocean Sciences; Canadian Inst. for Advanced Research (CIFAR), Toronto (Canada)
Publication Date:
Research Org.:
Monterey Bay Aquarium Research Inst., Moss Landing, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF); Gordon and Betty Moore Foundation
OSTI Identifier:
1346278
Alternate Identifier(s):
OSTI ID: 1366539
Grant/Contract Number:  
SC0004765; GBMF3788; IOS0843119
Resource Type:
Journal Article: Published Article
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 12; Journal Issue: 3; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Cuvelier, Marie L., Guo, Jian, Ortiz, Alejandra C., van Baren, Marijke J., Tariq, Muhammad Akram, Partensky, Frédéric, and Worden, Alexandra Z. Responses of the picoprasinophyte Micromonas commoda to light and ultraviolet stress. United States: N. p., 2017. Web. doi:10.1371/journal.pone.0172135.
Cuvelier, Marie L., Guo, Jian, Ortiz, Alejandra C., van Baren, Marijke J., Tariq, Muhammad Akram, Partensky, Frédéric, & Worden, Alexandra Z. Responses of the picoprasinophyte Micromonas commoda to light and ultraviolet stress. United States. doi:10.1371/journal.pone.0172135.
Cuvelier, Marie L., Guo, Jian, Ortiz, Alejandra C., van Baren, Marijke J., Tariq, Muhammad Akram, Partensky, Frédéric, and Worden, Alexandra Z. Thu . "Responses of the picoprasinophyte Micromonas commoda to light and ultraviolet stress". United States. doi:10.1371/journal.pone.0172135.
@article{osti_1346278,
title = {Responses of the picoprasinophyte Micromonas commoda to light and ultraviolet stress},
author = {Cuvelier, Marie L. and Guo, Jian and Ortiz, Alejandra C. and van Baren, Marijke J. and Tariq, Muhammad Akram and Partensky, Frédéric and Worden, Alexandra Z.},
abstractNote = {Micromonas is a unicellular marine green alga that thrives from tropical to polar ecosystems. We investigated the growth and cellular characteristics of acclimated mid-exponential phase Micromonas commoda RCC299 over multiple light levels and over the diel cycle (14:10 hour light:dark). We also exposed the light:dark acclimated M. commoda to experimental shifts from moderate to high light (HL), and to HL plus ultraviolet radiation (HL+UV), 4.5 hours into the light period. Cellular responses of this prasinophyte were quantified by flow cytometry and changes in gene expression by qPCR and RNA-seq. While proxies for chlorophyll a content and cell size exhibited similar diel variations in HL and controls, with progressive increases during day and decreases at night, both parameters sharply decreased after the HL+UV shift. Two distinct transcriptional responses were observed among chloroplast genes in the light shift experiments: i) expression of transcription and translation-related genes decreased over the time course, and this transition occurred earlier in treatments than controls; ii) expression of several photosystem I and II genes increased in HL relative to controls, as did the growth rate within the same diel period. However, expression of these genes decreased in HL+UV, likely as a photoprotective mechanism. RNA-seq also revealed two genes in the chloroplast genome, ycf2-like and ycf1-like, that had not previously been reported. The latter encodes the second largest chloroplast protein in Micromonas and has weak homology to plant Ycf1, an essential component of the plant protein translocon. Analysis of several nuclear genes showed that the expression of LHCSR2, which is involved in non-photochemical quenching, and five light-harvesting-like genes, increased 30 to >50-fold in HL+UV, but was largely unchanged in HL and controls. Under HL alone, a gene encoding a novel nitrite reductase fusion protein (NIRFU) increased, possibly reflecting enhanced N-assimilation under the 625 μmol photons m-2 s-1 supplied in the HL treatment. NIRFU's domain structure suggests it may have more efficient electron transfer than plant NIR proteins. Lastly, our analyses indicate that Micromonas can readily respond to abrupt environmental changes, such that strong photoinhibition was provoked by combined exposure to HL and UV, but a ca. 6-fold increase in light was stimulatory.},
doi = {10.1371/journal.pone.0172135},
journal = {PLoS ONE},
number = 3,
volume = 12,
place = {United States},
year = {Thu Mar 09 00:00:00 EST 2017},
month = {Thu Mar 09 00:00:00 EST 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1371/journal.pone.0172135

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Works referenced in this record:

Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus
journal, July 2009

  • Ito, H.; Mutsuda, M.; Murayama, Y.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 33, p. 14168-14173
  • DOI: 10.1073/pnas.0902587106