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

Loftus, Sarah E.; Johnson, Zackary I.

doi:10.3389/fbioe.2019.00101

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

Journal Article · Tue May 14 00:00:00 EDT 2019 · Frontiers in Bioengineering and Biotechnology

DOI:https://doi.org/10.3389/fbioe.2019.00101· OSTI ID:1613411

Loftus, Sarah E. ^[1]; Johnson, Zackary I. ^[2]

Duke Univ., Durham, NC (United States); DOE/OSTI
Duke Univ., Durham, NC (United States)

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.

View Accepted Manuscript (DOE)

Research Organization:: Duke Univ., Durham, NC (United States); Duke University, Durham, NC (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE Office of Energy Efficiency and Renewable Energy (EERE); USDOE Office of Energy Efficiency and Renewable Energy (EERE), Office of Sustainable Transportation. Bioenergy Technologies Office (BETO)

Grant/Contract Number:: EE0007091; EE0008518

OSTI ID:: 1613411

Alternate ID(s):: OSTI ID: 2439747

Journal Information:: Frontiers in Bioengineering and Biotechnology, Journal Name: Frontiers in Bioengineering and Biotechnology Vol. 7; ISSN 2296-4185

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (66)

Growth inhibition of Monodus subterraneus by free fatty acids Bosma, R.; Miazek, K.; Willemsen, S. M. Biotechnology and Bioengineering, Vol. 101, Issue 5 https://doi.org/10.1002/bit.21963	journal	December 2008
A chemical characterization of an algal inhibitor obtained from chlamydomonas McCracken, Michael D.; Middaugh, Robert E.; Middaugh, Randall S. Hydrobiologia, Vol. 70, Issue 3 https://doi.org/10.1007/bf00016771	journal	February 1980
Production, isolation and preliminary characterization of the exopolysaccharide of the cyanobacterium Spirulina platensis Filali Mouhim, R.; Cornet, J. -F.; Fontane, T. Biotechnology Letters, Vol. 15, Issue 6 https://doi.org/10.1007/bf00138541	journal	June 1993
Bacteria-organic matter coupling and its significance for oceanic carbon cycling Azam, F.; Smith, D. C.; Steward, G. F. Microbial Ecology, Vol. 28, Issue 2 https://doi.org/10.1007/bf00166806	journal	September 1994
Production and decomposition of new DOC by marine plankton communities: carbohydrates, refractory components and nutrient limitation Kragh, Theis; Søndergaard, Morten Biogeochemistry, Vol. 96, Issue 1-3 https://doi.org/10.1007/s10533-009-9357-1	journal	August 2009
Influence of culture medium recycling on the performance of Arthrospira platensis cultures Depraetere, Orily; Pierre, Guillaume; Noppe, Wim Algal Research, Vol. 10 https://doi.org/10.1016/j.algal.2015.04.014	journal	July 2015
Demonstrated large-scale production of marine microalgae for fuels and feed Huntley, Mark E.; Johnson, Zackary I.; Brown, Susan L. Algal Research, Vol. 10 https://doi.org/10.1016/j.algal.2015.04.016	journal	July 2015
Effects of cultivation conditions on the production of soluble algal products (SAPs) of Scenedesmus sp. LX1 Wu, Yin-Hu; Yu, Yin; Hu, Hong-Ying Algal Research, Vol. 16 https://doi.org/10.1016/j.algal.2016.04.006	journal	June 2016
Recycling Nannochloropsis oceanica culture media and growth inhibitors characterization Zhang, Xuezhi; Lu, Zhiying; Wang, Yifei Algal Research, Vol. 20 https://doi.org/10.1016/j.algal.2016.09.001	journal	December 2016
Cross-study analysis of factors affecting algae cultivation in recycled medium for biofuel production Loftus, Sarah E.; Johnson, Zackary I. Algal Research, Vol. 24 https://doi.org/10.1016/j.algal.2017.03.007	journal	June 2017
Cytotoxic effects of free fatty acids on phytoplankton algae and cyanobacteria Wu, Jiunn-Tzong; Chiang, Yin-Ru; Huang, Wen-Ya Aquatic Toxicology, Vol. 80, Issue 4 https://doi.org/10.1016/j.aquatox.2006.09.011	journal	December 2006
Dissolved organic matter (DOM) in microalgal photobioreactors: A potential loss in solar energy conversion? Hulatt, Chris J.; Thomas, David N. Bioresource Technology, Vol. 101, Issue 22 https://doi.org/10.1016/j.biortech.2010.06.086	journal	November 2010
The culture of Chlorella vulgaris in a recycled supernatant: Effects on biomass production and medium quality Hadj-Romdhane, F.; Zheng, X.; Jaouen, P. Bioresource Technology, Vol. 132 https://doi.org/10.1016/j.biortech.2013.01.025	journal	March 2013
Pilot-scale continuous recycling of growth medium for the mass culture of a halotolerant Tetraselmis sp. in raceway ponds under increasing salinity: A novel protocol for commercial microalgal biomass production Fon Sing, S.; Isdepsky, A.; Borowitzka, M. A. Bioresource Technology, Vol. 161 https://doi.org/10.1016/j.biortech.2014.03.010	journal	June 2014
Water use and its recycling in microalgae cultivation for biofuel application Farooq, Wasif; Suh, William I.; Park, Min S. Bioresource Technology, Vol. 184 https://doi.org/10.1016/j.biortech.2014.10.140	journal	May 2015
Roles of diatom nutrient stress and species identity in determining the short- and long-term bioavailability of diatom exudates to bacterioplankton Wear, Emma K.; Carlson, Craig A.; Windecker, Laura A. Marine Chemistry, Vol. 177 https://doi.org/10.1016/j.marchem.2015.09.001	journal	December 2015
Implementation of UV-based advanced oxidation processes in algal medium recycling Wang, Wenxuan; Sha, Jun; Lu, Zhiying Science of The Total Environment, Vol. 634 https://doi.org/10.1016/j.scitotenv.2018.03.342	journal	September 2018
Characterisation of algogenic organic matter extracted from cyanobacteria, green algae and diatoms Henderson, Rita K.; Baker, Andy; Parsons, Simon A. Water Research, Vol. 42, Issue 13 https://doi.org/10.1016/j.watres.2007.10.032	journal	July 2008
Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols Kolber, Zbigniew S.; Prášil, Ondřej; Falkowski, Paul G. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1367, Issue 1-3 https://doi.org/10.1016/s0005-2728(98)00135-2	journal	October 1998
Cyanobacterial reuse of extracellular organic carbon in microbial mats Stuart, Rhona K.; Mayali, Xavier; Lee, Jackson Z. The ISME Journal, Vol. 10, Issue 5 https://doi.org/10.1038/ismej.2015.180	journal	October 2015
Nutrient recycling facilitates long-term stability of marine microbial phototroph–heterotroph interactions Christie-Oleza, Joseph A.; Sousoni, Despoina; Lloyd, Matthew Nature Microbiology, Vol. 2, Issue 9 https://doi.org/10.1038/nmicrobiol.2017.100	journal	June 2017
Optimization of flocculation with tannin-based flocculant in the water reuse and lipidic production for the cultivation of Acutodesmus obliquus Hesse, M. C. S.; Santos, B.; Selesu, N. F. H. Separation Science and Technology, Vol. 52, Issue 5 https://doi.org/10.1080/01496395.2016.1269130	journal	December 2016
The biology of biofouling diatoms and their role in the development of microbial slimes Molino, Paul J.; Wetherbee, Richard Biofouling, Vol. 24, Issue 5 https://doi.org/10.1080/08927010802254583	journal	July 2008
Isolation and characterization of extracellular polysaccharides from the epipelic diatoms Cylindrotheca closterium and Navicula salinarum Staats, Natascha; De Winder, Ben; Stal, Lucas European Journal of Phycology, Vol. 34, Issue 2 https://doi.org/10.1080/09670269910001736212	journal	May 1999
The Use of Radio-active Carbon (C14) for Measuring Organic Production in the Sea Nielsen, E. S. ICES Journal of Marine Science, Vol. 18, Issue 2 https://doi.org/10.1093/icesjms/18.2.117	journal	August 1952
Identifying labile DOM components in a coastal ocean through depleted bacterial transcripts and chemical signals: Labile DOM in a coastal ocean Vorobev, Alexey; Sharma, Shalabh; Yu, Mengyun Environmental Microbiology, Vol. 20, Issue 8 https://doi.org/10.1111/1462-2920.14344	journal	July 2018
Biogenic Carbon Cycling in the Upper Ocean: Effects of Microbial Respiration Rivkin, R. B. Science, Vol. 291, Issue 5512 https://doi.org/10.1126/science.291.5512.2398	journal	March 2001
Bacterial Biovolume and Biomass Estimations Bratbak, Gunnar Applied and Environmental Microbiology, Vol. 49, Issue 6 https://doi.org/10.1128/aem.49.6.1488-1493.1985	journal	January 1985
Elemental Composition (C, N, P) and Cell Volume of Exponentially Growing and Nutrient-Limited Bacterioplankton Vrede, K.; Heldal, M.; Norland, S. Applied and Environmental Microbiology, Vol. 68, Issue 6 https://doi.org/10.1128/aem.68.6.2965-2971.2002	journal	June 2002
Bacterial Growth Efficiency in Natural Aquatic Systems del Giorgio, Paul A.; Cole, Jonathan J. Annual Review of Ecology and Systematics, Vol. 29, Issue 1 https://doi.org/10.1146/annurev.ecolsys.29.1.503	journal	November 1998
The morphology and molecular phylogenetics of some marine diatom taxa within the Fragilariaceae, including twenty undescribed species and their relationship to Nanofrustulum, Opephora and Pseudostaurosira Li, Chun L.; Witkowski, Andrzej; Ashworth, Matt P. Phytotaxa, Vol. 355, Issue 1 https://doi.org/10.11646/phytotaxa.355.1.1	journal	June 2018
The effect of iron- and light-limitation on phytoplankton communities of deep chlorophyll maxima of the western Pacific Ocean Johnson, Zackary I.; Shyam, Ragini; Ritchie, Anna E. Journal of Marine Research, Vol. 68, Issue 2 https://doi.org/10.1357/002224010793721433	journal	March 2010
Dissolved organic matter assimilation by heterotrophic bacterial groups in the western Arctic Ocean Elifantz, H.; Dittel, Ai; Cottrell, Mt Aquatic Microbial Ecology, Vol. 50 https://doi.org/10.3354/ame01145	journal	December 2007
Interactions of planktonic algae and bacteria: effects on algal growth and organic matter dynamics Grossart, Hp; Simon, M. Aquatic Microbial Ecology, Vol. 47 https://doi.org/10.3354/ame047163	journal	May 2007
Phytoplankton extracellular release and bacterial growth: dependence on the inorganic N: P ratio Obernosterer, I.; Herndl, Gj Marine Ecology Progress Series, Vol. 116 https://doi.org/10.3354/meps116247	journal	January 1995
A comparison between glass fiber and membrane filters for the estimation of phytoplankton POC and DOC production Morán, Xag; Gasol, Jm; Arin, L. Marine Ecology Progress Series, Vol. 187 https://doi.org/10.3354/meps187031	journal	January 1999
Description and application of the background irradiance gradient-single turnover fluorometer (BIG-STf) Johnson, Zi Marine Ecology Progress Series, Vol. 283 https://doi.org/10.3354/meps283073	journal	January 2004
Closely related phytoplankton species produce similar suites of dissolved organic matter Becker, Jamie W.; Berube, Paul M.; Follett, Christopher L. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00111	journal	March 2014
High Lipid Induction in Microalgae for Biodiesel Production Sharma, Kalpesh K.; Schuhmann, Holger; Schenk, Peer M. Energies, Vol. 5, Issue 5 https://doi.org/10.3390/en5051532	journal	May 2012
Steady state growth and ammonium uptake of a fast-growing marine diatom 1: Steady States ammonium kinetics Goldman, Joel C.; McCarthy, James J. Limnology and Oceanography, Vol. 23, Issue 4 https://doi.org/10.4319/lo.1978.23.4.0695	journal	July 1978
Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton Biddanda, Bopaiah; Benner, Ronald Limnology and Oceanography, Vol. 42, Issue 3 https://doi.org/10.4319/lo.1997.42.3.0506	journal	May 1997
Use of elemental composition to predict bioavailability of dissolved organic matter in a Georgia river Sun, L.; Perdue, E. M.; Meyer, J. L. Limnology and Oceanography, Vol. 42, Issue 4 https://doi.org/10.4319/lo.1997.42.4.0714	journal	June 1997
Interactions among dissolved organic carbon, microbial processes, and community structure in the mesopelagic zone of the northwestern Sargasso Sea Carlson, Craig A.; Giovannoni, Stephen J.; Hansell, Dennis A. Limnology and Oceanography, Vol. 49, Issue 4 https://doi.org/10.4319/lo.2004.49.4.1073	journal	July 2004
A high-throughput method to measure photosynthesis-irradiance curves of phytoplankton: Microphotosynthetron Johnson, Zackary I.; Sheldon, Tamara L. Limnology and Oceanography: Methods, Vol. 5, Issue 11 https://doi.org/10.4319/lom.2007.5.417	journal	November 2007
Microalgae Reused Growth Medium Experiments Dataset Loftus, Sarah; Johnson, Zackary figshare https://doi.org/10.6084/m9.figshare.7237553.v1	dataset	January 2018
Microalgae Reused Growth Medium Experiments Dataset Loftus, Sarah; Johnson, Zackary figshare https://doi.org/10.6084/m9.figshare.7237553.v2	dataset	January 2019
Understanding marine dissolved organic matter production: Compositional insights from axenic cultures of Thalassiosira pseudonana: T. Pseudonana-Derived DOM Saad, Emily M.; Longo, Amelia F.; Chambers, Luke R. Limnology and Oceanography, Vol. 61, Issue 6 https://doi.org/10.1002/lno.10367	journal	July 2016
A chemical characterization of an algal inhibitor obtained from chlamydomonas McCracken, Michael D.; Middaugh, Robert E.; Middaugh, Randall S. Hydrobiologia, Vol. 70, Issue 3 https://doi.org/10.1007/BF00016771	journal	February 1980
Production, isolation and preliminary characterization of the exopolysaccharide of the cyanobacterium Spirulina platensis Filali Mouhim, R.; Cornet, J. -F.; Fontane, T. Biotechnology Letters, Vol. 15, Issue 6 https://doi.org/10.1007/BF00138541	journal	June 1993
Bacteria-organic matter coupling and its significance for oceanic carbon cycling Azam, F.; Smith, D. C.; Steward, G. F. Microbial Ecology, Vol. 28, Issue 2 https://doi.org/10.1007/BF00166806	journal	September 1994
DOM Sources, Sinks, Reactivity, and Budgets Carlson, Craig A.; Hansell, Dennis A. Biogeochemistry of Marine Dissolved Organic Matter https://doi.org/10.1016/B978-0-12-405940-5.00003-0	book	October 2014
Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols Kolber, Zbigniew S.; Prášil, Ondřej; Falkowski, Paul G. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1367, Issue 1-3 https://doi.org/10.1016/S0005-2728(98)00135-2	journal	October 1998
Biological Activity of the Media After Algal Cultures can Result from Extracellular Carbohydrates Burkiewicz, Krystyna; Burkiewicz, Roman Journal of Plant Physiology, Vol. 148, Issue 6 https://doi.org/10.1016/S0176-1617(96)80364-6	journal	January 1996
Inhibitory effects of soluble algae products (SAP) released by Scenedesmus sp. LX1 on its growth and lipid production Zhang, Tian-Yuan; Yu, Yin; Wu, Yin-Hu Bioresource Technology, Vol. 146 https://doi.org/10.1016/j.biortech.2013.07.142	journal	October 2013
Air–Water Fluxes of N ₂ O and CH ₄ during Microalgae ( Staurosira sp.) Cultivation in an Open Raceway Pond Ferrón, Sara; Ho, David T.; Johnson, Zackary I. Environmental Science & Technology, Vol. 46, Issue 19 https://doi.org/10.1021/es302396j	journal	September 2012
A suite of microplate reader-based colorimetric methods to quantify ammonium, nitrate, orthophosphate and silicate concentrations for aquatic nutrient monitoring Ringuet, Stephanie; Sassano, Lara; Johnson, Zackary I. J. Environ. Monit., Vol. 13, Issue 2 https://doi.org/10.1039/C0EM00290A	journal	January 2011
Long-Term Cultivation of Algae in Open-Raceway Ponds: Lessons from the Field White, Rebecca L.; Ryan, Rebecca A. Industrial Biotechnology, Vol. 11, Issue 4 https://doi.org/10.1089/ind.2015.0006	journal	August 2015
Tracking differential incorporation of dissolved organic carbon types among diverse lineages of Sargasso Sea bacterioplankton: DOC incorporation by Sargasso Sea bacterioplankton Nelson, Craig E.; Carlson, Craig A. Environmental Microbiology, Vol. 14, Issue 6 https://doi.org/10.1111/j.1462-2920.2012.02738.x	journal	April 2012
Carbon allocation under light and nitrogen resource gradients in two model marine phytoplankton ¹ Bittar, Thais B.; Lin, Yajuan; Sassano, Lara R. Journal of Phycology, Vol. 49, Issue 3 https://doi.org/10.1111/jpy.12060	journal	March 2013
Bacterial Biovolume and Biomass Estimations Bratbak, Gunnar Applied and Environmental Microbiology, Vol. 49, Issue 6 https://doi.org/10.1128/AEM.49.6.1488-1493.1985	journal	January 1985
Elemental Composition (C, N, P) and Cell Volume of Exponentially Growing and Nutrient-Limited Bacterioplankton Vrede, K.; Heldal, M.; Norland, S. Applied and Environmental Microbiology, Vol. 68, Issue 6 https://doi.org/10.1128/AEM.68.6.2965-2971.2002	journal	June 2002
A simple and precise method for measuring ammonium in marine and freshwater ecosystems Holmes, Robert M.; Aminot, Alain; Kérouel, Roger Canadian Journal of Fisheries and Aquatic Sciences, Vol. 56, Issue 10 https://doi.org/10.1139/f99-128	journal	October 1999
Algae to Economically Viable Low-Carbon-Footprint Oil Bhujade, Ramesh; Chidambaram, Mandan; Kumar, Avnish Annual Review of Chemical and Biomolecular Engineering, Vol. 8, Issue 1 https://doi.org/10.1146/annurev-chembioeng-060816-101630	journal	June 2017
Dramatic Variability of the Carbonate System at a Temperate Coastal Ocean Site (Beaufort, North Carolina, USA) Is Regulated by Physical and Biogeochemical Processes on Multiple Timescales Johnson, Zackary I.; Wheeler, Benjamin J.; Blinebry, Sara K. PLoS ONE, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pone.0085117	journal	December 2013
Bacterial utilization of different size classes of dissolved organic matter Amon, Rainer M. W.; Benner, Ronald Limnology and Oceanography, Vol. 41, Issue 1 https://doi.org/10.4319/lo.1996.41.1.0041	journal	January 1996
Metabolic profiling reveals growth stage variability in diatom exudates: Exometabolome of diatoms Barofsky, Alexandra; Vidoudez, Charles; Pohnert, Georg Limnology and Oceanography: Methods, Vol. 7, Issue 6 https://doi.org/10.4319/lom.2009.7.382	journal	May 2009

Similar Records

Reused cultivation water from a self-inhibiting alga does not inhibit other algae but alters their microbiomes

Journal Article · Thu Sep 17 20:00:00 EDT 2020 · Algal Research · OSTI ID:1673383

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
algae biotechnology
algae cultivation
bacteria
biotechnology & applied microbiology
dissolved organic carbon
marine microalgae
recalcitrance
water reuse

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

Citation Formats

References (66)

Similar Records

Related Subjects