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Title: Reused Cultivation Water Accumulates Dissolved Organic Carbon and Uniquely Influences Different Marine Microalgae

Abstract

Reusing growth medium (water supplemented with nutrients) for microalgae cultivation is required for economical and environmentally sustainable production of algae bioproducts (fuels, feed, and food). However, reused medium often contains microbes and dissolved organic matter that may affect algae growth. While the accumulation of dissolved organic carbon (DOC) in reused medium has been demonstrated, it is unclear whether DOC concentrations affect algae growth or subsequent rates of algal DOC release. To address these questions, lab-scale experiments were conducted with three marine microalgae strains, Navicula sp. SFP, Staurosira sp. C323, and Chlorella sp. D046, grown in medium reused up to four times. Navicula sp. and Chlorella sp. grew similarly in reused medium as in fresh medium, while Staurosira sp. became completely inhibited in reused medium. Across the three algae, there was no broad trend between initial DOC concentration in reused medium and algae growth response. Navicula sp. released less DOC overall in reused medium than in fresh medium, but DOC release rates did not decrease proportionally with increased DOC concentrations. Net DOC accumulation was much lower than gross DOC released by Navicula sp. and Staurosira sp., indicating the majority of released DOC was degraded. Additionally, biodegradation experiments with reused media showedmore » no further net decrease in DOC, suggesting the accumulated DOC was recalcitrant to the associated bacteria. Overall, these results suggest that taxa-specific factors may be responsible for algae growth response in reused medium, and that DOC release and accumulation are insensitive to prior cultivation rounds. Choosing an algae strain that is uninhibited by accumulated DOC is therefore critical to ensure successful water reuse in the algae industry.« less

Authors:
 [1];  [1]
  1. Duke Univ., Durham, NC (United States)
Publication Date:
Research Org.:
Duke Univ., Durham, NC (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE); National Science Foundation (NSF)
OSTI Identifier:
1613411
Grant/Contract Number:  
EE0007091; 1644868
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Bioengineering and Biotechnology
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2296-4185
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biotechnology & applied microbiology; algae cultivation; water reuse; dissolved organic carbon; algae biotechnology; bacteria; marine microalgae; recalcitrance

Citation Formats

Loftus, Sarah E., and Johnson, Zackary I. Reused Cultivation Water Accumulates Dissolved Organic Carbon and Uniquely Influences Different Marine Microalgae. United States: N. p., 2019. Web. doi:10.3389/fbioe.2019.00101.
Loftus, Sarah E., & Johnson, Zackary I. Reused Cultivation Water Accumulates Dissolved Organic Carbon and Uniquely Influences Different Marine Microalgae. United States. https://doi.org/10.3389/fbioe.2019.00101
Loftus, Sarah E., and Johnson, Zackary I. Tue . "Reused Cultivation Water Accumulates Dissolved Organic Carbon and Uniquely Influences Different Marine Microalgae". United States. https://doi.org/10.3389/fbioe.2019.00101. https://www.osti.gov/servlets/purl/1613411.
@article{osti_1613411,
title = {Reused Cultivation Water Accumulates Dissolved Organic Carbon and Uniquely Influences Different Marine Microalgae},
author = {Loftus, Sarah E. and Johnson, Zackary I.},
abstractNote = {Reusing growth medium (water supplemented with nutrients) for microalgae cultivation is required for economical and environmentally sustainable production of algae bioproducts (fuels, feed, and food). However, reused medium often contains microbes and dissolved organic matter that may affect algae growth. While the accumulation of dissolved organic carbon (DOC) in reused medium has been demonstrated, it is unclear whether DOC concentrations affect algae growth or subsequent rates of algal DOC release. To address these questions, lab-scale experiments were conducted with three marine microalgae strains, Navicula sp. SFP, Staurosira sp. C323, and Chlorella sp. D046, grown in medium reused up to four times. Navicula sp. and Chlorella sp. grew similarly in reused medium as in fresh medium, while Staurosira sp. became completely inhibited in reused medium. Across the three algae, there was no broad trend between initial DOC concentration in reused medium and algae growth response. Navicula sp. released less DOC overall in reused medium than in fresh medium, but DOC release rates did not decrease proportionally with increased DOC concentrations. Net DOC accumulation was much lower than gross DOC released by Navicula sp. and Staurosira sp., indicating the majority of released DOC was degraded. Additionally, biodegradation experiments with reused media showed no further net decrease in DOC, suggesting the accumulated DOC was recalcitrant to the associated bacteria. Overall, these results suggest that taxa-specific factors may be responsible for algae growth response in reused medium, and that DOC release and accumulation are insensitive to prior cultivation rounds. Choosing an algae strain that is uninhibited by accumulated DOC is therefore critical to ensure successful water reuse in the algae industry.},
doi = {10.3389/fbioe.2019.00101},
journal = {Frontiers in Bioengineering and Biotechnology},
number = ,
volume = 7,
place = {United States},
year = {Tue May 14 00:00:00 EDT 2019},
month = {Tue May 14 00:00:00 EDT 2019}
}

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Works referenced in this record:

Dissolved organic matter assimilation by heterotrophic bacterial groups in the western Arctic Ocean
journal, December 2007

  • Elifantz, H.; Dittel, Ai; Cottrell, Mt
  • Aquatic Microbial Ecology, Vol. 50
  • DOI: 10.3354/ame01145

Isolation and characterization of extracellular polysaccharides from the epipelic diatoms Cylindrotheca closterium and Navicula salinarum
journal, May 1999


Demonstrated large-scale production of marine microalgae for fuels and feed
journal, July 2015


Biogenic Carbon Cycling in the Upper Ocean: Effects of Microbial Respiration
journal, March 2001


Influence of culture medium recycling on the performance of Arthrospira platensis cultures
journal, July 2015


Nutrient recycling facilitates long-term stability of marine microbial phototroph–heterotroph interactions
journal, June 2017


Recycling Nannochloropsis oceanica culture media and growth inhibitors characterization
journal, December 2016


Growth inhibition of Monodus subterraneus by free fatty acids
journal, December 2008

  • Bosma, R.; Miazek, K.; Willemsen, S. M.
  • Biotechnology and Bioengineering, Vol. 101, Issue 5
  • DOI: 10.1002/bit.21963

Metabolic profiling reveals growth stage variability in diatom exudates: Exometabolome of diatoms
journal, May 2009

  • Barofsky, Alexandra; Vidoudez, Charles; Pohnert, Georg
  • Limnology and Oceanography: Methods, Vol. 7, Issue 6
  • DOI: 10.4319/lom.2009.7.382

A simple and precise method for measuring ammonium in marine and freshwater ecosystems
journal, October 1999

  • Holmes, Robert M.; Aminot, Alain; Kérouel, Roger
  • Canadian Journal of Fisheries and Aquatic Sciences, Vol. 56, Issue 10
  • DOI: 10.1139/f99-128

Identifying labile DOM components in a coastal ocean through depleted bacterial transcripts and chemical signals: Labile DOM in a coastal ocean
journal, July 2018

  • Vorobev, Alexey; Sharma, Shalabh; Yu, Mengyun
  • Environmental Microbiology, Vol. 20, Issue 8
  • DOI: 10.1111/1462-2920.14344

Cross-study analysis of factors affecting algae cultivation in recycled medium for biofuel production
journal, June 2017


Bacteria-organic matter coupling and its significance for oceanic carbon cycling
journal, September 1994

  • Azam, F.; Smith, D. C.; Steward, G. F.
  • Microbial Ecology, Vol. 28, Issue 2
  • DOI: 10.1007/BF00166806

Interactions among dissolved organic carbon, microbial processes, and community structure in the mesopelagic zone of the northwestern Sargasso Sea
journal, July 2004

  • Carlson, Craig A.; Giovannoni, Stephen J.; Hansell, Dennis A.
  • Limnology and Oceanography, Vol. 49, Issue 4
  • DOI: 10.4319/lo.2004.49.4.1073

Bacterial Growth Efficiency in Natural Aquatic Systems
journal, November 1998


Cytotoxic effects of free fatty acids on phytoplankton algae and cyanobacteria
journal, December 2006


Interactions of planktonic algae and bacteria: effects on algal growth and organic matter dynamics
journal, May 2007


A comparison between glass fiber and membrane filters for the estimation of phytoplankton POC and DOC production
journal, January 1999

  • Morán, Xag; Gasol, Jm; Arin, L.
  • Marine Ecology Progress Series, Vol. 187
  • DOI: 10.3354/meps187031

Bacterial Biovolume and Biomass Estimations
journal, January 1985


A high-throughput method to measure photosynthesis-irradiance curves of phytoplankton: Microphotosynthetron
journal, November 2007

  • Johnson, Zackary I.; Sheldon, Tamara L.
  • Limnology and Oceanography: Methods, Vol. 5, Issue 11
  • DOI: 10.4319/lom.2007.5.417

A suite of microplate reader-based colorimetric methods to quantify ammonium, nitrate, orthophosphate and silicate concentrations for aquatic nutrient monitoring
journal, January 2011

  • Ringuet, Stephanie; Sassano, Lara; Johnson, Zackary I.
  • J. Environ. Monit., Vol. 13, Issue 2
  • DOI: 10.1039/C0EM00290A

Optimization of flocculation with tannin-based flocculant in the water reuse and lipidic production for the cultivation of Acutodesmus obliquus
journal, December 2016


Cyanobacterial reuse of extracellular organic carbon in microbial mats
journal, October 2015

  • Stuart, Rhona K.; Mayali, Xavier; Lee, Jackson Z.
  • The ISME Journal, Vol. 10, Issue 5
  • DOI: 10.1038/ismej.2015.180

A chemical characterization of an algal inhibitor obtained from chlamydomonas
journal, February 1980

  • McCracken, Michael D.; Middaugh, Robert E.; Middaugh, Randall S.
  • Hydrobiologia, Vol. 70, Issue 3
  • DOI: 10.1007/bf00016771

Water use and its recycling in microalgae cultivation for biofuel application
journal, May 2015


Use of elemental composition to predict bioavailability of dissolved organic matter in a Georgia river
journal, June 1997


Bacterial utilization of different size classes of dissolved organic matter
journal, January 1996


Air–Water Fluxes of N 2 O and CH 4 during Microalgae ( Staurosira sp.) Cultivation in an Open Raceway Pond
journal, September 2012

  • Ferrón, Sara; Ho, David T.; Johnson, Zackary I.
  • Environmental Science & Technology, Vol. 46, Issue 19
  • DOI: 10.1021/es302396j

Dissolved organic matter (DOM) in microalgal photobioreactors: A potential loss in solar energy conversion?
journal, November 2010


Understanding marine dissolved organic matter production: Compositional insights from axenic cultures of Thalassiosira pseudonana: T. Pseudonana-Derived DOM
journal, July 2016

  • Saad, Emily M.; Longo, Amelia F.; Chambers, Luke R.
  • Limnology and Oceanography, Vol. 61, Issue 6
  • DOI: 10.1002/lno.10367

Production, isolation and preliminary characterization of the exopolysaccharide of the cyanobacterium Spirulina platensis
journal, June 1993

  • Filali Mouhim, R.; Cornet, J. -F.; Fontane, T.
  • Biotechnology Letters, Vol. 15, Issue 6
  • DOI: 10.1007/BF00138541

The culture of Chlorella vulgaris in a recycled supernatant: Effects on biomass production and medium quality
journal, March 2013


Phytoplankton extracellular release and bacterial growth: dependence on the inorganic N: P ratio
journal, January 1995

  • Obernosterer, I.; Herndl, Gj
  • Marine Ecology Progress Series, Vol. 116
  • DOI: 10.3354/meps116247

Microalgae Reused Growth Medium Experiments Dataset
dataset, January 2018


Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton
journal, May 1997


Interactions among dissolved organic carbon, microbial processes, and community structure in the mesopelagic zone of the northwestern Sargasso Sea
journal, July 2004

  • Carlson, Craig A.; Giovannoni, Stephen J.; Hansell, Dennis A.
  • Limnology and Oceanography, Vol. 49, Issue 4
  • DOI: 10.4319/lo.2004.49.4.1073

Cytotoxic effects of free fatty acids on phytoplankton algae and cyanobacteria
journal, December 2006


Cross-study analysis of factors affecting algae cultivation in recycled medium for biofuel production
journal, June 2017


Optimization of flocculation with tannin-based flocculant in the water reuse and lipidic production for the cultivation of Acutodesmus obliquus
journal, December 2016


The biology of biofouling diatoms and their role in the development of microbial slimes
journal, July 2008


Recycling Nannochloropsis oceanica culture media and growth inhibitors characterization
journal, December 2016


The Use of Radio-active Carbon (C14) for Measuring Organic Production in the Sea
journal, August 1952


Steady state growth and ammonium uptake of a fast-growing marine diatom 1: Steady States ammonium kinetics
journal, July 1978


Long-Term Cultivation of Algae in Open-Raceway Ponds: Lessons from the Field
journal, August 2015

  • White, Rebecca L.; Ryan, Rebecca A.
  • Industrial Biotechnology, Vol. 11, Issue 4
  • DOI: 10.1089/ind.2015.0006

Algae to Economically Viable Low-Carbon-Footprint Oil
journal, June 2017


Nutrient recycling facilitates long-term stability of marine microbial phototroph–heterotroph interactions
journal, June 2017


Carbon allocation under light and nitrogen resource gradients in two model marine phytoplankton 1
journal, March 2013

  • Bittar, Thais B.; Lin, Yajuan; Sassano, Lara R.
  • Journal of Phycology, Vol. 49, Issue 3
  • DOI: 10.1111/jpy.12060

Inhibitory effects of soluble algae products (SAP) released by Scenedesmus sp. LX1 on its growth and lipid production
journal, October 2013


Description and application of the background irradiance gradient-single turnover fluorometer (BIG-STf)
journal, January 2004


Demonstrated large-scale production of marine microalgae for fuels and feed
journal, July 2015


Influence of culture medium recycling on the performance of Arthrospira platensis cultures
journal, July 2015


Cyanobacterial reuse of extracellular organic carbon in microbial mats
journal, October 2015

  • Stuart, Rhona K.; Mayali, Xavier; Lee, Jackson Z.
  • The ISME Journal, Vol. 10, Issue 5
  • DOI: 10.1038/ismej.2015.180

Closely related phytoplankton species produce similar suites of dissolved organic matter
journal, March 2014

  • Becker, Jamie W.; Berube, Paul M.; Follett, Christopher L.
  • Frontiers in Microbiology, Vol. 5
  • DOI: 10.3389/fmicb.2014.00111

Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols
journal, October 1998

  • Kolber, Zbigniew S.; Prášil, Ondřej; Falkowski, Paul G.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1367, Issue 1-3
  • DOI: 10.1016/S0005-2728(98)00135-2

Implementation of UV-based advanced oxidation processes in algal medium recycling
journal, September 2018


Biological Activity of the Media After Algal Cultures can Result from Extracellular Carbohydrates
journal, January 1996


Biogenic Carbon Cycling in the Upper Ocean: Effects of Microbial Respiration
journal, March 2001


Steady state growth and ammonium uptake of a fast-growing marine diatom 1: Steady States ammonium kinetics
journal, July 1978


Isolation and characterization of extracellular polysaccharides from the epipelic diatoms Cylindrotheca closterium and Navicula salinarum
journal, May 1999


Bacterial Growth Efficiency in Natural Aquatic Systems
journal, November 1998


A high-throughput method to measure photosynthesis-irradiance curves of phytoplankton: Microphotosynthetron
journal, November 2007

  • Johnson, Zackary I.; Sheldon, Tamara L.
  • Limnology and Oceanography: Methods, Vol. 5, Issue 11
  • DOI: 10.4319/lom.2007.5.417

High Lipid Induction in Microalgae for Biodiesel Production
journal, May 2012

  • Sharma, Kalpesh K.; Schuhmann, Holger; Schenk, Peer M.
  • Energies, Vol. 5, Issue 5
  • DOI: 10.3390/en5051532

Elemental Composition (C, N, P) and Cell Volume of Exponentially Growing and Nutrient-Limited Bacterioplankton
journal, June 2002


Interactions of planktonic algae and bacteria: effects on algal growth and organic matter dynamics
journal, May 2007


Dissolved organic matter (DOM) in microalgal photobioreactors: A potential loss in solar energy conversion?
journal, November 2010


Growth inhibition of Monodus subterraneus by free fatty acids
journal, December 2008

  • Bosma, R.; Miazek, K.; Willemsen, S. M.
  • Biotechnology and Bioengineering, Vol. 101, Issue 5
  • DOI: 10.1002/bit.21963

The effect of iron- and light-limitation on phytoplankton communities of deep chlorophyll maxima of the western Pacific Ocean
journal, March 2010

  • Johnson, Zackary I.; Shyam, Ragini; Ritchie, Anna E.
  • Journal of Marine Research, Vol. 68, Issue 2
  • DOI: 10.1357/002224010793721433

DOM Sources, Sinks, Reactivity, and Budgets
book, October 2014


Characterisation of algogenic organic matter extracted from cyanobacteria, green algae and diatoms
journal, July 2008


Identifying labile DOM components in a coastal ocean through depleted bacterial transcripts and chemical signals: Labile DOM in a coastal ocean
journal, July 2018

  • Vorobev, Alexey; Sharma, Shalabh; Yu, Mengyun
  • Environmental Microbiology, Vol. 20, Issue 8
  • DOI: 10.1111/1462-2920.14344

Dissolved organic matter assimilation by heterotrophic bacterial groups in the western Arctic Ocean
journal, December 2007

  • Elifantz, H.; Dittel, Ai; Cottrell, Mt
  • Aquatic Microbial Ecology, Vol. 50
  • DOI: 10.3354/ame01145

Phytoplankton extracellular release and bacterial growth: dependence on the inorganic N: P ratio
journal, January 1995

  • Obernosterer, I.; Herndl, Gj
  • Marine Ecology Progress Series, Vol. 116
  • DOI: 10.3354/meps116247

Use of elemental composition to predict bioavailability of dissolved organic matter in a Georgia river
journal, June 1997


The effect of iron- and light-limitation on phytoplankton communities of deep chlorophyll maxima of the western Pacific Ocean
journal, March 2010

  • Johnson, Zackary I.; Shyam, Ragini; Ritchie, Anna E.
  • Journal of Marine Research, Vol. 68, Issue 2
  • DOI: 10.1357/002224010793721433

The Use of Radio-active Carbon (C14) for Measuring Organic Production in the Sea
journal, August 1952


Characterisation of algogenic organic matter extracted from cyanobacteria, green algae and diatoms
journal, July 2008


Water use and its recycling in microalgae cultivation for biofuel application
journal, May 2015


The biology of biofouling diatoms and their role in the development of microbial slimes
journal, July 2008


Implementation of UV-based advanced oxidation processes in algal medium recycling
journal, September 2018


Closely related phytoplankton species produce similar suites of dissolved organic matter
journal, March 2014

  • Becker, Jamie W.; Berube, Paul M.; Follett, Christopher L.
  • Frontiers in Microbiology, Vol. 5
  • DOI: 10.3389/fmicb.2014.00111

High Lipid Induction in Microalgae for Biodiesel Production
journal, May 2012

  • Sharma, Kalpesh K.; Schuhmann, Holger; Schenk, Peer M.
  • Energies, Vol. 5, Issue 5
  • DOI: 10.3390/en5051532

Microalgae Reused Growth Medium Experiments Dataset
dataset, January 2018


The culture of Chlorella vulgaris in a recycled supernatant: Effects on biomass production and medium quality
journal, March 2013


Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton
journal, May 1997


Description and application of the background irradiance gradient-single turnover fluorometer (BIG-STf)
journal, January 2004


A comparison between glass fiber and membrane filters for the estimation of phytoplankton POC and DOC production
journal, January 1999

  • Morán, Xag; Gasol, Jm; Arin, L.
  • Marine Ecology Progress Series, Vol. 187
  • DOI: 10.3354/meps187031