Abstract
Rhodovulum sulfidophilum DSM-1374 is a potential producer of polyester when growing in phototrophic conditions. The present study investigated on a polyester product (P3HB) by culturing Rhodovulum sulfidophilum DSM-1374 in two different photobioreactors (PBR-1 and PBR-2) both with 4-L working volumes. PBR-1 is equipped with an internal rotor having 4 paddles to mix the bacterial culture while PBR-2 has an internal coil-shaped rotor. After selecting PBR-1, which best performed in the preliminary experiment, the effect of different stressing growth conditions as pH (7.0, 8.0, and 9.0), temperature (25, 30, and 35 °C), and medium salinity (1.5, 2.5, 3.5, and 4.5%) were tested. When the pH of the culture was set to 8.0, the capability of the bacterium to synthetize the polyester increased significantly reaching a concentration of 412 mg (P3HB)/L; the increase of the pH at 9.0 caused a reduction of the P3HB concentration in the culture. The medium salinity of 4.5% was the best stress-growth condition to reach the highest concentration of polyester in the culture (820 ± 50 mg (P3HB)/L) with a P3HB mass fraction in the dry biomass of 33 ± 1.5%. Stresses caused by culture temperature are another potential parameter that could increase the synthesis of P3HB.
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References
Anderson AJ, Dawes EA (1990) Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microbiol Rev 54(4):450–472
Cai J, Wang G (2012) Hydrogen production by a marine photosynthetic bacterium, Rhodovulum sulfidophilum P5, isolated from a shrimp pond. Int J Hydrog Energy 37:15070–15080. https://doi.org/10.1016/j.ijhydene.2012.07.130
Carlozzi P, Buccioni A, Minieri S, Pushparaj B, Piccardi R, Ena A, Pintucci C (2010) Production of bio-fuels (hydrogen and lipids) through a photofermentation process. Bioresour Technol 101:3115–3120. https://doi.org/10.1016/j.biortech.2009.12.049
Carlozzi P, Giovannelli A, Traversi ML, Touloupakis E, Di Lorenzo T (2019b) Poly-3-hydroxybutyrate and H2 production by Rhodopseudomonas sp. S16-VOGS3 grown in a new generation photobioreactor under single or combined nutrient deficiency. Int J Biol Macromol 135:821–828. https://doi.org/10.1016/j.ijbiomac.2019.05.220
Carlozzi P, Padovani G (2016) The aquatic fern Azolla as a natural plant-factory for ammonia removal from fish-breeding fresh wastewater. Environ Sci Pollut Res 23:8749–8755. https://doi.org/10.1007/s11356-016-6120-8
Carlozzi P, Pushparaj B, Degl’Innocenti A, Capperucci A (2006) Growth characteristics of Rhodopseudomonas palustris cultured outdoors, in an underwater tubular photobioreactor and investigation on photosynthetic efficiency. Appl Microbiol Biotechnol 73:789–795. https://doi.org/10.1007/s00253-006-0550-z
Carlozzi P, Seggiani M, Capperucci A, Tanini D, Cinelli P, Lazzeri A (2019a) Hydroxytyrosol rich-mixture from olive mill wastewater and production of green products by feeding Rhodopseudomonas sp. S16-FVPT5 with the residual effluent. J Biotechnol 295:28–36. https://doi.org/10.1016/j.jbiotec.2019.02.006
Carlozzi P, Seggiani M, Cinelli P, Mallegni N, Lazzeri A (2018) Photofermentative poly-3-hydroxybutyrate production by Rhodopseudomonas sp. S16-VOGS3 in a novel outdoor 70-L photobioreactor. Sustainability 10:3133. https://doi.org/10.3390/su10093133
Carlozzi P, Touloupakis E, Di Lorenzo T, Giovannelli A, Seggiani M, Cinelli P, Lazzeri A (2019c) Whey and molasses as inexpensive raw materials for parallel production of biohydrogen and polyesters via a two-stage bioprocess: new routes towards a circular bioeconomy. J Biotechnol 303:37–45. https://doi.org/10.1016/j.jbiotec.2019.07.008
Chen X, Yind J, Yea J, Zhang H, Che X, Ma Y, Li M, Wu LP, Chen GQ (2017) Engineering Halomonas bluephagenesis TD01 for non-sterile production of poly(3-hydroxybutyrate-co-4-hydroxybutyrate). Bioresour Technol 244:534–541. https://doi.org/10.1016/j.biortech.2017.07.149
Chowdhury WQ, Idehara K, Maeda I, Umeda F, Yagi K, Miura Y, Mizoguki T (1996) Factors affecting polyhydroxybutyrate biosynthesis in the marine photosynthetic bacterium Rhodopseudomonas sp. strain W-1S. Appl Biochem Biotechnol 57(58):361–366. https://doi.org/10.1007/978-1-4612-0223-3_31
CIEL (2017) Fossils, plastics, & petrochemical feedstocks. In Fueling Plastics, pp. 1–5, Center for International Environment Law
Cinelli P, Seggiani M, Mallegni N, Gigante V, Lazzeri A (2019) Processability and degradability of PHA-based composites in terrestrial environments. Int J Mol Sci 20:284. https://doi.org/10.3390/ijms20020284
Clemente T, Shah D, Tran M, Stark D, Padgette S, Dennis D, Brückener K, Steinbüchel A, Mitsky T (2000) Sequence of PHA synthase gene from two strains of Rhodospirillum rubrum and in vivo substrate specificity of four PHA synthases a cross two heterologous expression systems. Appl Microbiol Biotechnol 53:420–429. https://doi.org/10.1007/s002530051636
Higuchi-Takeuchi M, Morisaki K, Numata K (2016b) A screening method for the isolation of polyhydroxyalkanoate-producing purple non-sulfur photosynthetic bacteria from natural seawater. Front Microbiol 7:1509. https://doi.org/10.3389/fmicb.2016.01509
Higuchi-Takeuchi M, Morisaki K, Toyooka K, Numata K (2016a) Synthesis of high-molecular-weight polyhydroxyalkanoates by marine photosynthetic purple bacteria. PLoS One:1–17. https://doi.org/10.1371/journal.pone.0160981
Hiraishi A, Ueda Y (1994) Intrageneric structure of the genus Rhodobacter: transfer of Rhodobacter sulfiidophilus and related marine species to the genus Rhodovulum gen. nov. Int J Syst Bacteriol 44:15–23
Hustede E, Steinbükel A, Schlegel HG (1993) Relationship between the photoproduction of hydrogen and the accumulation of PHB in non-sulphur purple bacteria. Appl Microbiol Biotechnol 39:87–93. https://doi.org/10.1007/BF00166854
Khatipov E, Miyake M, Miyake J, Asada Y (1998) Accumulation of poly-β-hydroxybutyrate by Rhodobacter sphaeroides on various carbon and nitrogen substrates. FEMS Microbiol Lett 162:39–45. https://doi.org/10.1016/S0378-1097(98)00099-8
Kobayashi J, Kondo A (2019) Disruption of poly (3-hydroxyalkanoate) depolymerase gene and overexpression of three poly (3-hydroxybutyrate) biosynthetic genes improve poly (3-hydroxybutyrate) production from nitrogen rich medium by Rhodobacter sphaeroides. Microb Cell Factories 18:40. https://doi.org/10.1186/s12934-019-1088-y
Kranz RG, Gabbert KK, Locke TA, Madigan MT (1997) Polyhydroxyalkanoate production in Rhodobacter capsulatus: genes, mutants, expression, and physiology. Appl Environ Microbiol 63:3003–3009
Lorrungruang C, Martthong J, Sasaki K, Noparatnaraporn N (2006) Selection of photosynthetic bacterium Rhodobacter sphaeroides 14F for polyhydroxyalkanoate production with two-stage aerobic dark cultivation. J Biosci Bioeng 102:128–131. https://doi.org/10.1263/jbb.102.128
Maeda I, Chowdhury WQ, Idehara K, Yagi K, Mizoguchi T, Akano T, Miyasaka H, Furutani T, Ikuta Y, Shioji N, Miura Y (1998) Improvement of substrate conversion to molecular hydrogen by three-stage cultivation of a photosynthetic bacterium, Rhodovulum sulfidophilum. Appl Biochem Biotechnol 70-72:301–310. https://doi.org/10.1007/BF02920146
Martinez GA, Bertin L, Scoma A, Rebecchi S, Braunegg G, Fava F (2015) Production of polyhydroxyalkanoates from dephenolised and fermented olive mill wastewaters by employing a pure culture of Cupriavidus necator. Biochem Eng J 97:92–100. https://doi.org/10.1016/j.bej.2015.02.015
Melanie S, Winterburn JB, Devianto H (2018) Production of biopolymer polyhydroxyalkanoates (PHA) by extreme halophilic marine archaea Haloferax mediterranei in medium with varying phosphorus concentration. J Eng Technol Sci 50(2):255–271
Narancic T, Scollica E, Kenny ST, Gibbons H, Carr E, Brennan L, Cagney G, Wynne K, Murphy C, Raberg M, Heinrich D, Steinbüchel A, O’Connor K (2016) Understanding the physiological roles of polyhydroxybutyrate (PHB) in Rhodospirillum rubrum S1 under aerobic chemoheterotrophic conditions. Appl Microbiol Biotechnol 100(20):8901–8912. https://doi.org/10.1007/s00253-016-7711-5
Narancic T, Verstichel S, Reddy Chaganti S, Morales-Gamez L, Kenny ST, De Wilde B, Padamati RB, O’Connor KE (2018) Biodegradable plastic blends create new possibilities for end-of-life management of plastics but they are not a panacea for plastic pollution. Environ Sci Technol 52:10441–10452. https://doi.org/10.1021/acs.est.8b02963
Padovani G, Emiliani G, Giovanelli A, Traversi ML, Carlozzi P (2018) Assessment of glycerol usage by five different purple non-sulfur bacterial strains for bioplastic production. J Environ Chem Eng 6(1):616–622. https://doi.org/10.3390/su10093133
Poltronieri P, Kumar P (2017) Polyhydroxyalcanoates (PHAs) in industrial applications. In: L Kharissova O Kharisov B (eds) Handbook of Ecomaterials Martínez Switzerland: Springer, Cham pp 1-30. https://doi.org/10.1007/978-3-319-48281-1_70-1
Rutkowska M, Heimowska A, Krasowska K, Janik H (2002) Biodegradability of polyethylene starch blends in sea water. Pol Int J Environ Stud 11:267–272
Solaiman DKY, Ashby RD, Foglia TA, William N, Marmer WN (2006) Conversion of agricultural feedstock and coproducts into poly (hydroxyalkanoates). Appl Microbiol Biotechnol 71:783–789. https://doi.org/10.1007/s00253-006-0451-1
Suzuki T, Tsigankov AA, Miyake J, Tokiwa Y, Asada Y (1995) Accumulation of poly-(hydroxybutyrate) by a non-sulfur photosynthetic bacterium, Rhodobacter sphaeroides RV at different pH. Biotechnol Lett 17(4):395–400. https://doi.org/10.1007/BF00130796
Zhang J, Shishatskaya EI, Volova TG, Silva LF, Chen G-Q (2018) Polyhydroxyalkanoates (PHA) for therapeutic applications. Mater Sci Eng C 86:144–150. https://doi.org/10.1016/j.msec.2017.12.035
Acknowledgments
The authors would like to thank Marco De Vito (CNR-ISE) for the support in the analysis of samples.
Funding
This study was funded by the Regione Toscana, Italy, with the Project “ROBO-IMPLANT,” Bando FAS Salute 2014 (grant number 13299).
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Carlozzi, P., Di Lorenzo, T., Ghanotakis, D.F. et al. Effects of pH, temperature and salinity on P3HB synthesis culturing the marine Rhodovulum sulfidophilum DSM-1374. Appl Microbiol Biotechnol 104, 2007–2015 (2020). https://doi.org/10.1007/s00253-020-10352-1
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DOI: https://doi.org/10.1007/s00253-020-10352-1