Abstract
A new empirical model for the net oxygen production rate of an alkaliphilic microalgae consortium (AMC) with prominent members of Picochlorum and Pseudoanabaena was developed as a function of sulfide at concentrations up to 1.50 mM. The kinetic model consists of a non-continuous function with two domains for sulfide concentration, which describes the enhancement and the inhibition of net photosynthetic oxygen production. Small doses of sulfide can foster the photosynthetic activity evaluated by a Gaussian type of kinetic model; while, at a total sulfide concentration higher than 1.00 mM, the photosynthetic activity was inhibited following a linear inverse response. This study shows that small sulfide concentrations around 0.60 mM improved the photosynthetic activity by up to 90% compared to assays without sulfide. Moreover, the sulfide influence on the oxygenic photosynthetic activity of the AMC was confirmed after one year, suggesting that the kinetic model could be helpful for the design and operation of photobioreactors to improve the performance of microalgae cells exposed to hydrogen sulfide.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article and its supplementary information files.
References
APHA (2012) Standard Methods for the Examination of Water and Wastewater. Rice EW, Baird RB, Eaton AD, Clesceri LS (eds.) American Public Health Association (APHA).Washington, DC, USA, pp 724
Banciu HL, Muntyan MS (2015) Adaptive strategies in the double-extremophilic prokaryotes inhabiting soda lakes. Curr Opin Microbiol 25:73–79
Carvalho AP, Meireles LA, Malcata FX (2006) Microalgal reactors: a review of enclosed system designs and performances. Biotechnol Prog 22:1490–1506
Cheng J, Wang Z, Lu H, Xu J, He Y, Cen K (2019) Hydrogen Sulfide promotes cell division and photosynthesis of Nannochloropsis oceanica with 15% carbon dioxide. ACS Sustain Chem Eng 7:16344–16354
Cheng J, Wang Z, Lu H, Yang W, Fan Z (2020) Hydrogen sulfide improves lipid accumulation in Nannochloropsis oceanica through metabolic regulation of carbon allocation and energy supply. ACS Sustain Chem Eng 8:2481–2489
Cohen Y, Jørgensen BB, Revsbech NP, Poplawski R (1986) Adaptation to hydrogen sulfide of oxygenic and anoxygenic photosynthesis among cyanobacteria. Appl Environ Microbiol 51:398–407
De los Cobos-Vasconcelos D, García-Cruz EL, Franco-Morgado M, González-Sánchez A (2016) Short-term evaluation of the photosynthetic activity of an alkaliphilic microalgae consortium in a novel tubular closed photobioreactor. J Appl Phycol 28:795–802
de Wit R, Ende FP, Gemerden H (1995) Mathematical simulation of the interactions among cyanobacteria, purple sulfur bacteria and chemotrophic sulfur bacteria in microbial mat communities. FEMS Microbiol Ecol 17:117–136
Franco-Morgado M, Toledo-Cervantes A, González-Sánchez A, Lebrero R, Muñoz R (2018) Integral (VOCs, CO2, mercaptans and H2S) photosynthetic biogas upgrading using innovative biogas and digestate supply strategies. Chem Eng J 354:363–369
Giordano M, Prioretti L (2016) Sulphur and algae: Metabolism, ecology and evolution. In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 185–209
Giordano M, Raven JA (2014) Nitrogen and sulfur assimilation in plants and algae. Aquat Bot 118:45–61
González-Sánchez A, Posten C (2017) Fate of H2S during the cultivation of Chlorella sp. deployed for biogas upgrading. J Environ Manage 191:252–257
González-Sánchez A, Revah S (2007) The effect of chemical oxidation on the biological sulfide oxidation by an alkaliphilic sulfoxidizing bacterial consortium. Enzyme Microb Technol 40:292–298
Granada-Moreno CI, Aburto-Medina A, de los Cobos-Vasconcelos D, González-Sánchez A (2017) Microalgae community shifts during the biogas upgrading in an alkaline open photobioreactor. J Appl Microbiol 123:903–915
Griesbeck C, Hauska G, Schütz M (2000) Biological sulfide oxidation: sulfide-quinone reductase (SQR), the primary reaction. In: Pandalai SG (ed) Recent research developments in microbiology. Research Signpost, Trivadrum, India, pp 179–203
Hamilton TL, Klatt JM, De Beer D, Macalady JL (2018) Cyanobacterial photosynthesis under sulfidic conditions: insights from the isolate Leptolyngbya sp. strain hensonii. ISME J 12:568–584
Jennings ML (2013) Transport of H2S and HS- across the human red blood cell membrane: rapid H2S diffusion and AE1-mediated Cl-/HS- exchange. Am J Physiol Cell Physiol 305:C941–C950
Kazbar A, Cogne G, Urbain B, Marec H, Le-Gouic B, Tallec J, Pruvost J (2019) Effect of dissolved oxygen concentration on microalgal culture in photobioreactors. Algal Res 39:101432
Klatt JM, Haas S, Yilmaz P, de Beer D, Polerecky L (2015) Hydrogen sulfide can inhibit and enhance oxygenic photosynthesis in a cyanobacterium from sulphidic springs. Environ Microbiol 17:3301–3313
Kliphuis AM, Janssen M, van den End EJ, Martens DE, Wijffels RH (2011) Light respiration in Chlorella sorokiniana. J Appl Phycol 23:935–947
Kwon G, Le LT, Jeon J, Noh J, Jang Y, Kang D, Jahng D (2020) Effects of light and mass ratio of microalgae and nitrifiers on the rates of ammonia oxidation and nitrate production. Biochem Eng J 1:107656
Meier L, Stará D, Bartacek J, Jeison D (2018) Removal of H2S by a continuous microalgae-based photosynthetic biogas upgrading process. Process Saf Environ Prot 119:65–68
Miller SR, Bebout BM (2004) Variation in sulfide tolerance of photosystem II in phylogenetically diverse cyanobacteria from sulfidic habitats. Appl Environ Microbiol 70:736–744
Myers J, Graham JR (1971) The photosynthetic unit in Chlorella measured by repetitive short flashes. Plant Physiol 48:282–286
Nagarajan A, Pakrasi HB (2016) Membrane-bound protein complexes for photosynthesis and respiration in cyanobacteria. eLS, John Wiley & Sons, Ltd. https://doi.org/10.1002/9780470015902.a0001670.pub2
Puhakka JA, Ferguson JF, Benjamin MM, Salkinoja-Salonen M (1989) Sulfur reduction and inhibition in anaerobic treatment of simulated pulp mill wastewater. Syst Appl Microbiol 11:202–206
Ramírez-Rueda A, Velasco A, González-Sánchez A (2020) The effect of chemical sulfide oxidation on the oxygenic activity of an alkaliphilic microalgae consortium deployed for biogas upgrading. Sustainability 12:6610
Schwerna P, Hübner H, Buchholz R (2017) Quantification of oxygen production and respiration rates in mixotrophic cultivation of microalgae in nonstirred photobioreactors. Eng Life Sci 17:140–144
Sforza E, Pastore M, Franke SM, Barbera E (2020) Modeling the oxygen inhibition in microalgae: an experimental approach based on photorespirometry. New Biotechnol 59:26–32
Toro-Huertas EI, Franco-Morgado M, de los Cobos Vasconcelos D, González-Sánchez A (2019) Photorespiration in an outdoor alkaline open-photobioreactor used for biogas upgrading. Sci Total Environ 667:613–621
Acknowledgements
This study was financed by DGAPA-IT100121. The technical support of Daniel de los Cobos Vasconcelos, Margarita Elizabeth Cisneros Ortíz and Roberto Sotero Briones Méndez, is highly appreciated. This research work was performed in the Environmental Engineering Laboratory (LIA), Institute of Engineering UNAM, which holds an ISO 9001:2015 certificate.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Álvarez-Olivares, M., Velasco, A. & González-Sánchez, A. Kinetics of net photosynthetic oxygen production of a microalgae suspension at small doses of sulfide. J Appl Phycol 34, 2401–2408 (2022). https://doi.org/10.1007/s10811-022-02800-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-022-02800-4