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Title: Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform

Abstract

Background: The feasibility of heterotrophic–phototrophic symbioses was tested via pairing of yeast strains Cryptococcus curvatus, Rhodotorula glutinis, or Saccharomyces cerevisiae with a sucrose-secreting cyanobacterium Synechococcus elongatus. Results: The phototroph S. elongatus showed no growth in standard BG-11 medium with yeast extract, but grew well in BG-11 medium alone or supplemented with yeast nitrogen base without amino acids (YNB w/o aa). Among three yeast species, C. curvatus and R. glutinis adapted well to the BG-11 medium supplemented with YNB w/o aa, sucrose, and various concentrations of NaCl needed to maintain sucrose secretion from S. elongatus, while growth of S. cerevisiae was highly dependent on sucrose levels. R. glutinis and C. curvatus grew efficiently and utilized sucrose produced by the partner in co-culture. Co-cultures of S. elongatus and R. glutinis were sustained over 1 month in both batch and in semi-continuous culture, with the fnal biomass and overall lipid yields in the batch co-culture 40 to 60% higher compared to batch mono-cultures of S. elongatus. The co-cultures showed enhanced levels of palmitoleic and linoleic acids. Furthermore, cyanobacterial growth in co-culture with R. glutinis was signifcantly superior to axenic growth, as S. elongatus was unable to grow in the absence of the yeastmore » partner when cultivated at lower densities in liquid medium. Accumulated reactive oxygen species was observed to severely inhibit axenic growth of cyanobacteria, which was efficiently alleviated through catalase supply and even more effectively with co-cultures of R. glutinis. Conclusions: The pairing of a cyanobacterium and eukaryotic heterotroph in the artifcial lichen of this study demonstrates the importance of mutual interactions between phototrophs and heterotrophs, e.g., phototrophs provide a carbon source to heterotrophs, and heterotrophs assist phototrophic growth and survival by removing/eliminating oxidative stress. Our results establish a potential stable production platform that combines the metabolic capability of photoautotrophs to capture inorganic carbon with the channeling of the resulting organic carbon directly to a robust heterotroph partner for producing biofuel and other chemical precursors.« less

Authors:
; ; ; ; ; ;
Publication Date:
Research Org.:
National Renewable Energy Laboratory (NREL), Golden, CO (United States); Johns Hopkins Univ., Baltimore, MD (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE)
OSTI Identifier:
1618671
Alternate Identifier(s):
OSTI ID: 1351861; OSTI ID: 1485587
Report Number(s):
NREL/JA-5100-68306
Journal ID: ISSN 1754-6834; 55; PII: 736
Grant/Contract Number:  
DE‐SC0012658; SC0012658; AC36-08GO28308
Resource Type:
Published Article
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Name: Biotechnology for Biofuels Journal Volume: 10 Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
Springer Science + Business Media
Country of Publication:
Netherlands
Language:
English
Subject:
09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; cyanobacteria; yeasts; co-culture; sucrose; ROS; artificial lichen; hydrogen peroxide; lipid production; Co‑culture; Artifcial lichen

Citation Formats

Li, Tingting, Li, Chien-Ting, Butler, Kirk, Hays, Stephanie G., Guarnieri, Michael T., Oyler, George A., and Betenbaugh, Michael J. Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform. Netherlands: N. p., 2017. Web. doi:10.1186/s13068-017-0736-x.
Li, Tingting, Li, Chien-Ting, Butler, Kirk, Hays, Stephanie G., Guarnieri, Michael T., Oyler, George A., & Betenbaugh, Michael J. Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform. Netherlands. https://doi.org/10.1186/s13068-017-0736-x
Li, Tingting, Li, Chien-Ting, Butler, Kirk, Hays, Stephanie G., Guarnieri, Michael T., Oyler, George A., and Betenbaugh, Michael J. Tue . "Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform". Netherlands. https://doi.org/10.1186/s13068-017-0736-x.
@article{osti_1618671,
title = {Mimicking lichens: incorporation of yeast strains together with sucrose-secreting cyanobacteria improves survival, growth, ROS removal, and lipid production in a stable mutualistic co-culture production platform},
author = {Li, Tingting and Li, Chien-Ting and Butler, Kirk and Hays, Stephanie G. and Guarnieri, Michael T. and Oyler, George A. and Betenbaugh, Michael J.},
abstractNote = {Background: The feasibility of heterotrophic–phototrophic symbioses was tested via pairing of yeast strains Cryptococcus curvatus, Rhodotorula glutinis, or Saccharomyces cerevisiae with a sucrose-secreting cyanobacterium Synechococcus elongatus. Results: The phototroph S. elongatus showed no growth in standard BG-11 medium with yeast extract, but grew well in BG-11 medium alone or supplemented with yeast nitrogen base without amino acids (YNB w/o aa). Among three yeast species, C. curvatus and R. glutinis adapted well to the BG-11 medium supplemented with YNB w/o aa, sucrose, and various concentrations of NaCl needed to maintain sucrose secretion from S. elongatus, while growth of S. cerevisiae was highly dependent on sucrose levels. R. glutinis and C. curvatus grew efficiently and utilized sucrose produced by the partner in co-culture. Co-cultures of S. elongatus and R. glutinis were sustained over 1 month in both batch and in semi-continuous culture, with the fnal biomass and overall lipid yields in the batch co-culture 40 to 60% higher compared to batch mono-cultures of S. elongatus. The co-cultures showed enhanced levels of palmitoleic and linoleic acids. Furthermore, cyanobacterial growth in co-culture with R. glutinis was signifcantly superior to axenic growth, as S. elongatus was unable to grow in the absence of the yeast partner when cultivated at lower densities in liquid medium. Accumulated reactive oxygen species was observed to severely inhibit axenic growth of cyanobacteria, which was efficiently alleviated through catalase supply and even more effectively with co-cultures of R. glutinis. Conclusions: The pairing of a cyanobacterium and eukaryotic heterotroph in the artifcial lichen of this study demonstrates the importance of mutual interactions between phototrophs and heterotrophs, e.g., phototrophs provide a carbon source to heterotrophs, and heterotrophs assist phototrophic growth and survival by removing/eliminating oxidative stress. Our results establish a potential stable production platform that combines the metabolic capability of photoautotrophs to capture inorganic carbon with the channeling of the resulting organic carbon directly to a robust heterotroph partner for producing biofuel and other chemical precursors.},
doi = {10.1186/s13068-017-0736-x},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 10,
place = {Netherlands},
year = {Tue Mar 21 00:00:00 EDT 2017},
month = {Tue Mar 21 00:00:00 EDT 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1186/s13068-017-0736-x

Citation Metrics:
Cited by: 47 works
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Figures / Tables:

Fig. 1 Fig. 1: Axenic growth of different yeast strains. a–c Effect of medium components on monoculture of yeasts; “BG” indicates BG-11 added with 2 g/L sucrose, 4 mM ammonium chloride, 1 mM IPTG, and 100 mM NaCl; “BG + YNB w/o aa” indicates “BG” supplied with YNB w/o aa; “BG +more » YE” indicates “BG” supplied with YE. d–f Effect of glucose/sucrose and light/dark on monoculture of yeasts; Medium used here was BG-11[co] supplied with 2 g/L sucrose or 2 g/L glucose, as indicated in the legends. g–i Effect of sucrose concentration on monoculture of yeasts; Medium used here was BG-11[co] supplied with various concentration of sucrose, as indicated in the legends. j–l Effect of NaCl concentration on monoculture of yeasts. Medium here was BG-11[co] supplied with 2 g/L sucrose, but with adjusted NaCl concentration in each condition. a, d, g, j for C. curvatus; b, e, h, k for R. glutinis; c, f, i, l for S. cerevisiae. Light condition was used if no specific statement. All data are averages of biological triplicates ± standard deviation« less

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Works referenced in this record:

High-cell-density cultivation of the lipid accumulating yeast Cryptococcus curvatus using glycerol as a carbon source
journal, June 1996

  • Meesters, P. A. E. P.; Huijberts, G. N. M.; Eggink, G.
  • Applied Microbiology and Biotechnology, Vol. 45, Issue 5
  • DOI: 10.1007/s002530050731

Growth promotion of Chlorella ellipsoidea by co-inoculation with Brevundimonas sp. isolated from the microalga
journal, September 2007


Oil production by oleaginous yeasts using the hydrolysate from pretreatment of wheat straw with dilute sulfuric acid
journal, May 2011


Enhanced Lipid Production by Co-cultivation and Co-encapsulation of Oleaginous Yeast Trichosporonoides spathulata with Microalgae in Alginate Gel Beads
journal, March 2014

  • Kitcha, Suleeporn; Cheirsilp, Benjamas
  • Applied Biochemistry and Biotechnology, Vol. 173, Issue 2
  • DOI: 10.1007/s12010-014-0859-5

Inhibitory effect of oxygen accumulation on the growth of Spirulina platensis
journal, February 1995

  • Marquez, Facundo J.; Sasaki, Ken; Nishio, Naomichi
  • Biotechnology Letters, Vol. 17, Issue 2
  • DOI: 10.1007/BF00127993

A New Strategy for Lipid Production by Mix Cultivation of Spirulina platensis and Rhodotorula glutinis
journal, October 2008

  • Xue, Feiyan; Miao, Jinxin; Zhang, Xu
  • Applied Biochemistry and Biotechnology, Vol. 160, Issue 2
  • DOI: 10.1007/s12010-008-8376-z

Correction: Sucrose Utilization in Budding Yeast as a Model for the Origin of Undifferentiated Multicellularity
journal, August 2011


Direct quantification of fatty acids in wet microalgal and yeast biomass via a rapid in situ fatty acid methyl ester derivatization approach
journal, August 2015


Yarrowia lipolytica as a model for bio-oil production
journal, November 2009

  • Beopoulos, Athanasios; Cescut, Julien; Haddouche, Ramdane
  • Progress in Lipid Research, Vol. 48, Issue 6, p. 375-387
  • DOI: 10.1016/j.plipres.2009.08.005

Role of pretreatment and conditioning processes on toxicity of lignocellulosic biomass hydrolysates
journal, June 2009


Continuous hydrogen peroxide production by organic buffers in phytoplankton culture media
journal, October 2013

  • Jeffrey Morris, J.; Zinser, Erik R.
  • Journal of Phycology, Vol. 49, Issue 6
  • DOI: 10.1111/jpy.12123

Engineering cyanobacteria as photosynthetic feedstock factories
journal, February 2014


Effects of nitrate and oxygen on photoautotrophic lipid production from Chlorococcum littorale
journal, February 2011


Interaction between cyanobacteria and aerobic heterotrophic bacteria in the degradation of hydrocarbons
journal, January 2010


Synthetic photosynthetic consortia define interactions leading to robustness and photoproduction
journal, January 2017

  • Hays, Stephanie G.; Yan, Leo L. W.; Silver, Pamela A.
  • Journal of Biological Engineering, Vol. 11, Issue 1
  • DOI: 10.1186/s13036-017-0048-5

Oxidative Stability of Polyunsaturated Triacylglycerols Encapsulated in Oleaginous Yeast
journal, June 2008

  • Iassonova, Diliara R.; Hammond, Earl G.; Beattie, Samuel E.
  • Journal of the American Oil Chemists' Society, Vol. 85, Issue 8
  • DOI: 10.1007/s11746-008-1255-5

Exploring the photosynthetic production capacity of sucrose by cyanobacteria
journal, September 2013


Microbial production of fatty-acid-derived fuels and chemicals from plant biomass
journal, January 2010

  • Steen, Eric J.; Kang, Yisheng; Bokinsky, Gregory
  • Nature, Vol. 463, Issue 7280, p. 559-562
  • DOI: 10.1038/nature08721

Mixed culture of oleaginous yeast Rhodotorula glutinis and microalga Chlorella vulgaris for lipid production from industrial wastes and its use as biodiesel feedstock
journal, July 2011

  • Cheirsilp, Benjamas; Suwannarat, Warangkana; Niyomdecha, Rujira
  • New Biotechnology, Vol. 28, Issue 4
  • DOI: 10.1016/j.nbt.2011.01.004

Ecological and biotechnological aspects of lichens
journal, November 2006


Rerouting Carbon Flux To Enhance Photosynthetic Productivity
journal, February 2012

  • Ducat, Daniel C.; Avelar-Rivas, J. Abraham; Way, Jeffrey C.
  • Applied and Environmental Microbiology, Vol. 78, Issue 8
  • DOI: 10.1128/AEM.07901-11

Light-dependent generation of reactive oxygen species in cell culture media
journal, June 2001

  • Grzelak, Agnieszka; Rychlik, Błażej; Bartosz, Grzegorz
  • Free Radical Biology and Medicine, Vol. 30, Issue 12
  • DOI: 10.1016/S0891-5849(01)00545-7

Inference of interactions in cyanobacterial–heterotrophic co-cultures via transcriptome sequencing
journal, April 2014

  • Beliaev, Alexander S.; Romine, Margie F.; Serres, Margrethe
  • The ISME Journal, Vol. 8, Issue 11
  • DOI: 10.1038/ismej.2014.69

Lipid Production by Culturing Oleaginous Yeast and Algae with Food Waste and Municipal Wastewater in an Integrated Process
journal, May 2011

  • Chi, Zhanyou; Zheng, Yubin; Jiang, Anping
  • Applied Biochemistry and Biotechnology, Vol. 165, Issue 2
  • DOI: 10.1007/s12010-011-9263-6

Oily yeasts as oleaginous cell factories
journal, April 2011

  • Ageitos, Jose Manuel; Vallejo, Juan Andres; Veiga-Crespo, Patricia
  • Applied Microbiology and Biotechnology, Vol. 90, Issue 4
  • DOI: 10.1007/s00253-011-3200-z

The potential for agro-industrial waste utilization using oleaginous yeast for the production of biodiesel
journal, May 2014


Early Molecular Investigations of Lichen-Forming Symbionts: 1986–2001
journal, October 2004


Symbiotic association in Chlorella culture
journal, January 2005


Oil production by the yeast Trichosporon dermatis cultured in enzymatic hydrolysates of corncobs
journal, April 2012


Growth of Chlamydomonas reinhardtii in acetate-free medium when co-cultured with alginate-encapsulated, acetate-producing strains of Synechococcus sp. PCC 7002
journal, October 2014

  • Therien, Jesse B.; Zadvornyy, Oleg A.; Posewitz, Matthew C.
  • Biotechnology for Biofuels, Vol. 7, Issue 1
  • DOI: 10.1186/s13068-014-0154-2

Cyanobacteria in Symbiosis
book, January 2002


Oxidative Stress Responses in the Unicellular Cyanobacterium Synechococcus Pcc 7942
journal, January 1991


Engineering Cyanobacteria To Synthesize and Export Hydrophilic Products
journal, April 2010

  • Niederholtmeyer, H.; Wolfstadter, B. T.; Savage, D. F.
  • Applied and Environmental Microbiology, Vol. 76, Issue 11
  • DOI: 10.1128/AEM.00202-10

Response of Prochlorococcus ecotypes to co-culture with diverse marine bacteria
journal, February 2011

  • Sher, Daniel; Thompson, Jessie W.; Kashtan, Nadav
  • The ISME Journal, Vol. 5, Issue 7
  • DOI: 10.1038/ismej.2011.1

Works referencing / citing this record:

Co-culturing of oleaginous microalgae and yeast: paradigm shift towards enhanced lipid productivity
journal, April 2019

  • Arora, Neha; Patel, Alok; Mehtani, Juhi
  • Environmental Science and Pollution Research, Vol. 26, Issue 17
  • DOI: 10.1007/s11356-019-05138-6

Opportunities and challenges in the development of Cutaneotrichosporon oleaginosus ATCC 20509 as a new cell factory for custom tailored microbial oils
journal, October 2017

  • Bracharz, Felix; Beukhout, Teun; Mehlmer, Norbert
  • Microbial Cell Factories, Vol. 16, Issue 1
  • DOI: 10.1186/s12934-017-0791-9

Engineering microbial consortia by division of labor
journal, February 2019


Photoautotrophic production of polyhydroxyalkanoates in a synthetic mixed culture of Synechococcus elongatus cscB and Pseudomonas putida cscAB
journal, July 2017


Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.