Increased Growth of the Microalga Chlorella vulgaris when Coimmobilized and Cocultured in Alginate Beads with the Plant-Growth-Promoting Bacterium Azospirillum brasilense
Open accessAbstract
Coimmobilization of the freshwater microalga Chlorella vulgaris and the plant-growth-promoting bacterium Azospirillum brasilense in small alginate beads resulted in a significantly increased growth of the microalga. Dry and fresh weight, total number of cells, size of the microalgal clusters (colonies) within the bead, number of microalgal cells per cluster, and the levels of microalgal pigments significantly increased. Light microscopy revealed that both microorganisms colonized the same cavities inside the beads, though the microalgae tended to concentrate in the more aerated periphery while the bacteria colonized the entire bead. The effect of indole-3-acetic acid addition to microalgal culture prior to immobilization of microorganisms in alginate beads partially imitated the effect of A. brasilense. We propose that coimmobilization of microalgae and plant-growth-promoting bacteria is an effective means of increasing microalgal populations within confined environments.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The co-immobilization of the microorganisms resulted in increments of up to 35% in chlorophyll a, 176% in chlorophyll b, 186% in ß-carotene, 152% in lutein, and 129% in violaxanthin.
“The co-immobilization of the microorganisms resulted in increments of up to 35% in chlorophyll a, 176% in chlorophyll b, 186% in ß-carotene, 152% in lutein, and 129% in violaxanthin [87].”
From Toward the Enhancement of Microalgal Metabolite Production through Microalgae–Bacteria Consortia (2021) · cites this paper as [87]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The enhancement of plant growth by free-living bacteria
Glick, B. R. (1995) · Canadian Journal of Microbiology · doi:10.1139/m95-015 · Cited by 2,669 · see citing works
Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria
Kloepper, J. W., Leong, J., Teintze, M., & Schroth, M. N. (1980) · Nature · doi:10.1038/286885a0 · Cited by 1,561 · see citing works
Bacterial biosynthesis of indole-3-acetic acid
Patten, C. L., & Glick, B. R. (1996) · Canadian Journal of Microbiology · doi:10.1139/m96-032 · Cited by 1,234 · see citing works
Bashan, Y., Holguín, G., & de‐Bashan, L. E. (2004) · Canadian Journal of Microbiology · doi:10.1139/w04-035 · Cited by 937 · see citing works
Self-citationBorowitzka, M. A. (1998) · Springer eBooks · doi:10.1007/978-3-662-10863-5_12 · Cited by 856 · see citing works
Inoculants of plant growth-promoting bacteria for use in agriculture
Bashan, Y. (1998) · Biotechnology Advances · doi:10.1016/s0734-9750(98)00003-2 · Cited by 808 · see citing works
Self-citationAgronomic applications of azospirillum: An evaluation of 20 years worldwide field inoculation
Okon, Y., & Labandera-Gonzalez, C. A. (1994) · Soil Biology and Biochemistry · doi:10.1016/0038-0717(94)90311-5 · Cited by 720 · see citing works
Azospirillum– plant relationships: environmental and physiological advances (1990–1996)
Bashan, Y., & Holguín, G. (1997) · Canadian Journal of Microbiology · doi:10.1139/m97-015 · Cited by 617 · see citing works
Self-citationSynthesis of Phytohormones by Plant-Associated Bacteria
Costacurta, A., & Vanderleyden, J. (1995) · Critical Reviews in Microbiology · doi:10.3109/10408419509113531 · Cited by 606 · see citing works
Borowitzka, M. A., & Borowitzka, L. J. (2021) · Royal Society of Chemistry eBooks · doi:10.1039/9781839162473 · Cited by 568 · see citing works
Environmental applications of immobilized microbial cells: A review
Cassidy, M., Lee, H., & Trevors, J. T. (1996) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/bf01570068 · Cited by 560 · see citing works
Astaxanthin from Microbial Sources
Johnson, E. A., & An, G.-H. (1991) · Critical Reviews in Biotechnology · doi:10.3109/07388559109040622 · Cited by 509 · see citing works
Bioremoval of heavy metals by the use of microalgae
Wilde, E. W., & Benemann, J. R. (1993) · Biotechnology Advances · doi:10.1016/0734-9750(93)90003-6 · Cited by 479 · see citing works
Bashan, Y., & Holguín, G. (1998) · Soil Biology and Biochemistry · doi:10.1016/s0038-0717(97)00187-9 · Cited by 439 · see citing works
Self-citationCurrent status of Azospirillum inoculation technology: Azospirillum as a challenge for agriculture
Bashan, Y., & Levanony, H. (1990) · Canadian Journal of Microbiology · doi:10.1139/m90-105 · Cited by 380 · see citing works
Self-citationGonzalez, L. E., Cañizares, R., & Baena, S. (1997) · Bioresource Technology · doi:10.1016/s0960-8524(97)00029-1 · Cited by 369 · see citing works
Self-citationAlginate Beads as Synthetic Inoculant Carriers for Slow Release of Bacteria That Affect Plant Growth
Bashan, Y. (1986) · Applied and Environmental Microbiology · doi:10.1128/aem.51.5.1089-1098.1986 · Cited by 325 · see citing works
Self-citationThe potential of microalgal biotechnology: A review of production and uses of microalgae
de la Noüe, J., & Pauw, N. D. (1988) · Biotechnology Advances · doi:10.1016/0734-9750(88)91921-0 · Cited by 267 · see citing works
Degradation of phenol by polymer entrapped microorganisms
Bettmann, H., & Rehm, H. J. (1984) · Applied Microbiology and Biotechnology · doi:10.1007/bf00270587 · Cited by 250 · see citing works
Vidussi, F., Claustre, H., Bustillos-Guzmán, J. J., Cailliau, C., & Marty, J. (1996) · Journal of Plankton Research · doi:10.1093/plankt/18.12.2377 · Cited by 220 · see citing works
Leenen, E. J. T. M., dos Santos, V. A. P. M., Grolle, K., et al. (1996) · Water Research · doi:10.1016/s0043-1354(96)00209-6 · Cited by 186 · see citing works
Wastewater Nutrients (N and P) Removal by Carrageenan and Alginate Immobilized Chlorella Vulgaris
Lau, A. P. S., Tam, N. F. Y., & Wong, Y. S. (1997) · Environmental Technology · doi:10.1080/09593331808616614 · Cited by 183 · see citing works
Methods in Plant Molecular Biology and Biotechnology
Glick, B. R. (2018) · CRC Press eBooks · doi:10.1201/9781351074490 · Cited by 128 · see citing works
Isolation and Characterization of Plant Growth-Promoting Rhizobacteria
Bashan, Y., Holguín, G., & Lifshitz, R. (1993) · Cited by 126 · see citing works
Self-citationHolguín, G., & Bashan, Y. (1996) · Soil Biology and Biochemistry · doi:10.1016/s0038-0717(96)00251-9 · Cited by 112 · see citing works
Self-citationBioreactor Immobilized Enzymes and Cells: Fundamentals and Applications
Moo‐Young, M. (1988) · Medical Entomology and Zoology · Cited by 109 · see citing works
Wastewater inorganic N and P removal by immobilized chlorella vulgaris
Tam, N. F. Y., Lau, A. P. S., & Wong, Y. S. (1994) · Water Science & Technology · doi:10.2166/wst.1994.0288 · Cited by 79 · see citing works
Root-to-Root Travel of the Beneficial Bacterium Azospirillum brasilense
Bashan, Y., & Holguín, G. (1994) · Applied and Environmental Microbiology · doi:10.1128/aem.60.6.2120-2131.1994 · Cited by 77 · see citing works
Self-citationPuente, M. E., Holguín, G., Glick, B. R., et al. (1999) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.1999.tb00619.x · Cited by 75 · see citing works
An Industrial View of Azospirillum Inoculants: Formulation and Application Technology
Fages, J. (1992) · DalSpace (Dalhousie University) · Cited by 75 · see citing works
Defined coimmobilization of mixed microorganism cultures
O'Reilly, A. M., & Scott, J. A. (1995) · Enzyme and Microbial Technology · doi:10.1016/0141-0229(94)00103-x · Cited by 63 · see citing works
Formation of ?-keto acids from amino acids using immobilized bacteria and algae
Wikstr�m, P., Szwajcer, E., Brodelius, P. E., Nilsson, K., & Mosbach, K. (1982) · Biotechnology Letters · doi:10.1007/bf00144316 · Cited by 57 · see citing works
Dibb-Fuller, J., & Morris, D. (1992) · Planta · doi:10.1007/bf00196251 · Cited by 49 · see citing works
Bashan, Y., Levanony, H., & Ziv-Vecht, O. (1987) · Canadian Journal of Microbiology · doi:10.1139/m87-188 · Cited by 48 · see citing works
Self-citationKaya, V. M., de la Noüe, J., & Picard, G. (1995) · Journal of Applied Phycology · doi:10.1007/bf00003556 · Cited by 48 · see citing works
Application of immobilized growing cells
Tanaka, A., & Nakajima, H. (2005) · Springer eBooks · doi:10.1007/bfb0000732 · Cited by 41 · see citing works
Denitrification by Azospirillum brasilense Sp 7
Zimmer, W., Stephan, M. P., & Bothe, H. (1984) · Archives of Microbiology · doi:10.1007/bf00402121 · Cited by 38 · see citing works
Bajguz, A., & Czerpak, R. (1996) · Journal of Plant Growth Regulation · doi:10.1007/bf00198931 · Cited by 37 · see citing works
Denitrification by Azospirillum brasilense Sp 7
Stephan, M. P., Zimmer, W., & Bothe, H. (1984) · Archives of Microbiology · doi:10.1007/bf00402122 · Cited by 35 · see citing works
Oxygen diffusion through gels employed for immobilization
Omar, S. (1993) · Applied Microbiology and Biotechnology · doi:10.1007/bf00170419 · Cited by 32 · see citing works
Oxygen diffusion through gels employed for immobilization
Omar, S. (1993) · Applied Microbiology and Biotechnology · doi:10.1007/bf00170362 · Cited by 31 · see citing works
Behavior of algae and bacteria co-immobilized in carrageenan, in a fluidized bed
Chevalier, P., & de la Noüe, J. (1988) · Enzyme and Microbial Technology · doi:10.1016/0141-0229(88)90093-2 · Cited by 24 · see citing works
Hydrogen evolution by co-immobilized Chlorella vulgaris and Clostridium butyricum cells
Kayano, H., Matsunaga, T., Karube, I., & Suzuki, S. (1981) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/0005-2728(81)90188-2 · Cited by 22 · see citing works
Enhanced ?-lactam antibiotic production by coimmobilization of fungus and alga
Khang, Y. H., Shankar, H., & Senatora, F. (1988) · Biotechnology Letters · doi:10.1007/bf01026997 · Cited by 17 · see citing works
Interactions between Azospirillum and Arthrobacter in diazotrophic mixed culture
Lippi, D., Cacciari, I., Pietrosanti, T., et al. (1992) · DalSpace (Dalhousie University) · Cited by 16 · see citing works
Are Angiosperm Hormones Present in, and Used as Hormones by, Algae?
Jacobs, W. P. (1986) · Proceedings in life sciences · doi:10.1007/978-3-642-71018-6_32 · Cited by 9 · see citing works
Continuous Culture Application in Physiological Investigations on Diazotrophic Bacteria
Ueckert, J., & Fendrik, I. (1995) · Springer eBooks · doi:10.1007/978-3-642-79906-8_31 · Cited by 4 · see citing works
Flagged first, then by citations
Research works printed but not linked: 10
- [10]Becker E W. Micro-algae for human and animal consumption. In: Borowitzka M A, Borowitzka L J, editors. Micro-algal biotechnology. Cambridge, United Kingdom: Cambridge University Press; 1992. pp. 222–256. [Google Scholar]
- [12]Borowitzka M A, Borowitzka L J, editors. Micro-algal biotechnology. Cambridge, United Kingdom: Cambridge University Press; 1992. [Google Scholar]
- [17]De Pauw N, Persoone G. Micro-algae for aquaculture. In: Borowitzka M A, Borowitzka L J, editors. Micro-algal biotechnology. Cambridge, United Kingdom: Cambridge University Press; 1992. pp. 197–221. [Google Scholar]
- [22]Hartmann A, Zimmer W. Physiology of Azospirillum. In: Okon Y, editor. Azospirillum/plant associations. Boca Raton, Fla: CRC Press; 1994. pp. 15–39. [Google Scholar]
- [33]Metting B. Micro-algae in agriculture. In: Borowitzka M A, Borowitzka L J, editors. Micro-algal biotechnology. Cambridge, United Kingdom: Cambridge University Press; 1992. pp. 288–304. [Google Scholar]
- [35]Ogoshi A, Kobayashi K, Homma Y, Kodama F, Kondo N, Akino S, editors. Plant growth-promoting bacteria—present status and future prospects. Sapporo, Japan: Hokkaido University Press; 1997. [Google Scholar]
- [36]Oh-Hama T, Miyachi S. Chlorella. In: Borowitzka M A, Borowitzka L J, editors. Micro-algal biotechnology. Cambridge, United Kingdom: Cambridge University Press; 1992. pp. 3–26. [Google Scholar]
- [40]Oswald W J. Micro-algae and waste-water treatment. In: Borowitzka M A, Borowitzka L J, editors. Micro-algal biotechnology. Cambridge, United Kingdom: Cambridge University Press; 1992. pp. 305–328. [Google Scholar]
- [50]Zhulin I B, Armitage J P. The role of taxis in the ecology of Azospirillum. Symbiosis. 1992;13:199–206. [Google Scholar]
- [51]Zimmer W, Stephan M P, Bothe H. Denitrification by Azospirillum brasilense Sp7. I. Growth with nitrate as respiratory electron acceptor. Arch Microbiol. 1984;138:206–211. [Google Scholar]
Cited by
Sorted by citations
Algae-bacteria interactions: Evolution, ecology and emerging applications
Ramanan, R., Kim, B.-H., Cho, D.-H., Oh, H.-M., & Kim, H.-S. (2016) · Biotechnology Advances · doi:10.1016/j.biotechadv.2015.12.003 · Cited by 1,301 · see citing works
‘Morphology, composition, production, processing and applications of Chlorella vulgaris: a review’.
Safi, C., Zebib, B., Merah, O., Pontalier, P.-Y., & Vaca-Garcia, C. (2014) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2014.04.007 · Cited by 1,127 · see citing works
Integrating micro-algae into wastewater treatment: a review
Mohsenpour, S. F., Hennige, S., Willoughby, N., Adeloye, A., & Gutierrez, T. (2021) · Science of The Total Environment · doi:10.1016/j.scitotenv.2020.142168 · Cited by 828 · see citing works
Methods of downstream processing for the production of biodiesel from microalgae
Kim, J., Yoo, G., Lee, H., Lim, J., Kim, K., Kim, C. W., Park, M. S., & Yang, J.-W. (2013) · Biotechnology Advances · doi:10.1016/j.biotechadv.2013.04.006 · Cited by 519 · see citing works
Fuentes, J., Garbayo, I., Cuaresma, M., Montero, Z., González-del-Valle, M., & Vílchez, C. (2016) · Marine Drugs · doi:10.3390/md14050100 · Cited by 462 · see citing works
Conversion of Microalgae to Biofuel
Suali, E., & Sarbatly, R. (2012) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2012.03.047 · Cited by 456 · see citing works
Industrial potential of carotenoid pigments from microalgae: Current trends and future prospects
Ambati, R. R., Gogisetty, D., Aswathanarayana, R. G., Ravi, S., Bikkina, P. N., Bo, L., & Yuepeng, S. (2019) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2018.1432561 · Cited by 372 · see citing works
Enhancing microalgal biomass productivity by engineering a microalgal-bacterial community
Cho, D.-H., Ramanan, R., Heo, J., Lee, J., Kim, B.-H., Oh, H.-M., & Kim, H.-S. (2015) · Bioresource Technology · doi:10.1016/j.biortech.2014.10.159 · Cited by 305 · see citing works
de-Bashan, L. E., Bashan, Y., Moreno, M., Lebsky, V. K., & Bustillos, J. J. (2002) · Canadian Journal of Microbiology · doi:10.1139/w02-051 · Cited by 222 · see citing works
Self-citationRemoval of nitrogen from wastewater using microalgae and microalgae–bacteria consortia
Jia, H., & Yuan, Q. (2016) · Cogent Environmental Science · doi:10.1080/23311843.2016.1275089 · Cited by 216 · see citing works
Ma, X., Zhou, W., Fu, Z., Cheng, Y., Min, M., Liu, Y., Zhang, Y., Chen, P., & Ruan, R. (2014) · Bioresource Technology · doi:10.1016/j.biortech.2014.05.087 · Cited by 197 · see citing works
Xu, J., Zhao, Y., Zhao, G., & Zhang, H. (2015) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-015-6537-x · Cited by 172 · see citing works
Park, Y., Je, K.-W., Lee, K., Jung, S.-E., & Choi, T.-J. (2008) · Hydrobiologia · doi:10.1007/s10750-007-9152-8 · Cited by 150 · see citing works
Makut, B. B., Das, D., & Goswami, G. (2019) · Algal Research · doi:10.1016/j.algal.2018.11.020 · Cited by 137 · see citing works
Choix, F. J., de-Bashan, L. E., & Bashan, Y. (2012) · Enzyme and Microbial Technology · doi:10.1016/j.enzmictec.2012.07.012 · Cited by 133 · see citing works
Self-citationToward the Enhancement of Microalgal Metabolite Production through Microalgae–Bacteria Consortia
González-González, L. M., & de-Bashan, L. E. (2021) · Biology · doi:10.3390/biology10040282 · Cited by 133 · see citing works
Wang, H., Hill, R. T., Zheng, T., Hu, X., & Wang, B. (2016) · Critical Reviews in Biotechnology · doi:10.3109/07388551.2014.961402 · Cited by 131 · see citing works
Amavizca, E., Bashan, Y., Ryu, C.-M., Farag, M. A., Bebout, B. M., & de-Bashan, L. E. (2017) · Scientific Reports · doi:10.1038/srep41310 · Cited by 119 · see citing works
Self-citationEmerging Applications of Chlorella sp. and Spirulina (Arthrospira) sp.
Abreu, A. P., Martins, R., & Nunes, J. (2023) · Bioengineering · doi:10.3390/bioengineering10080955 · Cited by 119 · see citing works
Wang, H., Laughinghouse, H. D., Anderson, M. A., Chen, F., Willliams, E., Place, A. R., Zmora, O., Zohar, Y., Zheng, T., & Hill, R. T. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.06474-11 · Cited by 102 · see citing works
Trejo, A., de-Bashan, L. E., Hartmann, A., Hernandez, J.-P., Rothballer, M., Schmid, M., & Bashan, Y. (2012) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2011.08.007 · Cited by 82 · see citing works
Self-citationde-Bashan, L. E., Mayali, X., Bebout, B. M., Weber, P. K., Detweiler, A. M., Hernandez, J. P., Prufert-Bebout, L., & Bashan, Y. (2016) · Algal Research · doi:10.1016/j.algal.2016.02.019 · Cited by 79 · see citing works
Self-citationChoix, F. J., de-Bashan, L. E., & Bashan, Y. (2012) · Enzyme and Microbial Technology · doi:10.1016/j.enzmictec.2012.07.013 · Cited by 72 · see citing works
Meza, B., de-Bashan, L. E., & Bashan, Y. (2015) · Research in Microbiology · doi:10.1016/j.resmic.2014.12.010 · Cited by 61 · see citing works
Choix, F. J., Bashan, Y., Mendoza, A., & de-Bashan, L. E. (2014) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2014.02.014 · Cited by 56 · see citing works
Self-citationEnhancing Digestibility of Chlorella vulgaris Biomass in Monogastric Diets: Strategies and Insights
Spínola, M. P., Costa, M. M., & Prates, J. A. M. (2023) · Animals · doi:10.3390/ani13061017 · Cited by 45 · see citing works
Lopez, B. R., Bashan, Y., Trejo, A., & de-Bashan, L. E. (2013) · Biology and Fertility of Soils · doi:10.1007/s00374-013-0799-1 · Cited by 38 · see citing works
Self-citationLeyva, L. A., Bashan, Y., & de-Bashan, L. E. (2015) · Annals of Microbiology · doi:10.1007/s13213-014-0866-3 · Cited by 34 · see citing works
Self-citationSaputri, D. A. E., Prabaningtyas, S., & Aridowi, D. (2025) · AIP Conference Proceedings · doi:10.1063/5.0234821 · Cited by 1 · see citing works
- Authors
- Gonzalez, L. E., & Bashan, Y.
- Affiliations
- Pontificia Universidad Javeriana (CO)
- <!--label omitted: 2-->The Center for Biological Research of the Northwest (CIB), La Paz, B.C.S. 23000, Mexico2
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 2000-04
- Volume
- 66
- Issue
- 4
- Pages
- 1527-1531
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- PMC
- PMC92018
- OpenAlex
- W2160852650
- Cited by
- 304
- References
- 47
- Citations by year
- 2026: 9 · 2025: 9 · 2024: 13 · 2023: 22 · 2022: 19 · 2021: 25 · 2020: 15 · 2019: 21 · 2018: 21 · 2017: 13 · 2016: 14 · 2015: 21 · 2014: 14 · 2013: 17 · 2012: 14
- FWCI
- 4.43
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Applied and Environmental Microbiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Keywords
- Chlorella vulgaris, Azospirillum brasilense, alginate beads, co-immobilization, co-culture, plant growth-promoting bacteria, microalgae growth, indole-3-acetic acid, microalgal pigments
- MeSH terms
- Alginates, Chlorella, Culture Media, Hexuronic Acids, Microspheres, Pigments, Biological, Water Microbiology, Azospirillum brasilense, Waste Management, Cells, Immobilized, Glucuronic Acid
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
