Establishment of stable synthetic mutualism without co-evolution between microalgae and bacteria demonstrated by mutual transfer of metabolites (NanoSIMS isotopic imaging) and persistent physical association (Fluorescent in situ hybridization)
Abstract
The demonstration of a mutualistic interaction requires evidence of benefits for both partners as well as stability of the association over multiple generations. A synthetic mutualism between the freshwater microalga Chlorella sorokiniana and the soil-derived plant growth-promoting bacterium (PGPB) Azospirillum brasilense was created when both microorganisms were co-immobilized in alginate beads. Using stable isotope enrichment experiments followed by high-resolution secondary ion mass spectrometry (SIMS) imaging of single cells, we demonstrated transfer of carbon and nitrogen compounds between the two partners. Further, using fluorescent in situ hybridization (FISH), mechanical disruption and scanning electron microscopy, we demonstrated the stability of their physical association for a period of 10 days after the aggregated cells were released from the beads. The bacteria significantly enhanced the growth of the microalgae while the microalgae supported growth of the bacteria in a medium where it could not otherwise grow. In conclusion, we propose that this microalga-bacterium association is a true synthetic mutualism independent of co-evolution. (155 words).
- Authors:
-
- The Bashan Institute of Science, Auburn, AL (United States); Auburn Univ., AL (United States); Environmental Microbiology Group, Northwestern center for Biological Research, La Paz (Mexico)
- Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
- NASA Ames Research Center (ARC), Moffett Field, Mountain View, CA (United States)
- NASA Ames Research Center (ARC), Moffett Field, Mountain View, CA (United States); Bay Area Environmental Research Inst. Petaluma, CA (United States)
- The Bashan Institute of Science, Auburn, AL (United States); Environmental Microbiology Group, Northwestern center for Biological Research, La Paz (Mexico)
- The Bashan Institute of Science, Auburn, AL (United States)
- Publication Date:
- Research Org.:
- Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1241994
- Alternate Identifier(s):
- OSTI ID: 1356676
- Report Number(s):
- LLNL-JRNL-675179
Journal ID: ISSN 2211-9264
- Grant/Contract Number:
- AC52-07NA27344; SCW1039
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Algal Research
- Additional Journal Information:
- Journal Volume: 15; Journal Issue: C; Journal ID: ISSN 2211-9264
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; microalgae; NanoSIMS; plant growth-promoting bacteria; synthetic mutualism
Citation Formats
de-Bashan, Luz E., Mayali, Xavier, Bebout, Brad M., Weber, Peter K., Detweiler, Angela M., Hernandez, Juan- Pablo, Prufert-Bebout, Leslie, and Bashan, Yoav. Establishment of stable synthetic mutualism without co-evolution between microalgae and bacteria demonstrated by mutual transfer of metabolites (NanoSIMS isotopic imaging) and persistent physical association (Fluorescent in situ hybridization). United States: N. p., 2016.
Web. doi:10.1016/j.algal.2016.02.019.
de-Bashan, Luz E., Mayali, Xavier, Bebout, Brad M., Weber, Peter K., Detweiler, Angela M., Hernandez, Juan- Pablo, Prufert-Bebout, Leslie, & Bashan, Yoav. Establishment of stable synthetic mutualism without co-evolution between microalgae and bacteria demonstrated by mutual transfer of metabolites (NanoSIMS isotopic imaging) and persistent physical association (Fluorescent in situ hybridization). United States. https://doi.org/10.1016/j.algal.2016.02.019
de-Bashan, Luz E., Mayali, Xavier, Bebout, Brad M., Weber, Peter K., Detweiler, Angela M., Hernandez, Juan- Pablo, Prufert-Bebout, Leslie, and Bashan, Yoav. Thu .
"Establishment of stable synthetic mutualism without co-evolution between microalgae and bacteria demonstrated by mutual transfer of metabolites (NanoSIMS isotopic imaging) and persistent physical association (Fluorescent in situ hybridization)". United States. https://doi.org/10.1016/j.algal.2016.02.019. https://www.osti.gov/servlets/purl/1241994.
@article{osti_1241994,
title = {Establishment of stable synthetic mutualism without co-evolution between microalgae and bacteria demonstrated by mutual transfer of metabolites (NanoSIMS isotopic imaging) and persistent physical association (Fluorescent in situ hybridization)},
author = {de-Bashan, Luz E. and Mayali, Xavier and Bebout, Brad M. and Weber, Peter K. and Detweiler, Angela M. and Hernandez, Juan- Pablo and Prufert-Bebout, Leslie and Bashan, Yoav},
abstractNote = {The demonstration of a mutualistic interaction requires evidence of benefits for both partners as well as stability of the association over multiple generations. A synthetic mutualism between the freshwater microalga Chlorella sorokiniana and the soil-derived plant growth-promoting bacterium (PGPB) Azospirillum brasilense was created when both microorganisms were co-immobilized in alginate beads. Using stable isotope enrichment experiments followed by high-resolution secondary ion mass spectrometry (SIMS) imaging of single cells, we demonstrated transfer of carbon and nitrogen compounds between the two partners. Further, using fluorescent in situ hybridization (FISH), mechanical disruption and scanning electron microscopy, we demonstrated the stability of their physical association for a period of 10 days after the aggregated cells were released from the beads. The bacteria significantly enhanced the growth of the microalgae while the microalgae supported growth of the bacteria in a medium where it could not otherwise grow. In conclusion, we propose that this microalga-bacterium association is a true synthetic mutualism independent of co-evolution. (155 words).},
doi = {10.1016/j.algal.2016.02.019},
journal = {Algal Research},
number = C,
volume = 15,
place = {United States},
year = {Thu Mar 03 00:00:00 EST 2016},
month = {Thu Mar 03 00:00:00 EST 2016}
}
Web of Science
Works referenced in this record:
Azospirillum -plant relationships: physiological, molecular, agricultural, and environmental advances (1997-2003)
journal, August 2004
- Bashan, Yoav; Holguin, Gina; de-Bashan, Luz E.
- Canadian Journal of Microbiology, Vol. 50, Issue 8
Chlorella sorokiniana (formerly C. vulgaris) UTEX 2714, a non-thermotolerant microalga useful for biotechnological applications and as a reference strain
journal, April 2015
- Bashan, Yoav; Lopez, Blanca R.; Huss, Volker A. R.
- Journal of Applied Phycology, Vol. 28, Issue 1
Development of two culture media for mass cultivation of Azospirillum spp. and for production of inoculants to enhance plant growth
journal, April 2011
- Bashan, Yoav; Trejo, Adan; de-Bashan, Luz E.
- Biology and Fertility of Soils, Vol. 47, Issue 8
Engineering microbial consortia: a new frontier in synthetic biology
journal, September 2008
- Brenner, Katie; You, Lingchong; Arnold, Frances H.
- Trends in Biotechnology, Vol. 26, Issue 9, p. 483-489
Speciation by symbiosis
journal, August 2012
- Brucker, Robert M.; Bordenstein, Seth R.
- Trends in Ecology & Evolution, Vol. 27, Issue 8
Enhanced accumulation of starch and total carbohydrates in alginate-immobilized Chlorella spp. induced by Azospirillum brasilense: I. Autotrophic conditions
journal, October 2012
- Choix, Francisco J.; de-Bashan, Luz E.; Bashan, Yoav
- Enzyme and Microbial Technology, Vol. 51, Issue 5
Enhanced accumulation of starch and total carbohydrates in alginate-immobilized Chlorella spp. induced by Azospirillum brasilense: II. Heterotrophic conditions
journal, October 2012
- Choix, Francisco J.; de-Bashan, Luz E.; Bashan, Yoav
- Enzyme and Microbial Technology, Vol. 51, Issue 5
Enhanced activity of ADP glucose pyrophosphorylase and formation of starch induced by Azospirillum brasilense in Chlorella vulgaris
journal, May 2014
- Choix, Francisco J.; Bashan, Yoav; Mendoza, Alberto
- Journal of Biotechnology, Vol. 177
Applicability of the fluorescein diacetate method of detecting active bacteria in freshwater
journal, June 1984
- Chrzanowski, Thomas H.; Crotty, Rhonda D.; Hubbard, James G.
- Microbial Ecology, Vol. 10, Issue 2
The Domain-specific Probe EUB338 is Insufficient for the Detection of all Bacteria: Development and Evaluation of a more Comprehensive Probe Set
journal, September 1999
- Daims, Holger; Brühl, Andreas; Amann, Rudolf
- Systematic and Applied Microbiology, Vol. 22, Issue 3
Joint Immobilization of Plant Growth-Promoting Bacteria and Green Microalgae in Alginate Beads as an Experimental Model for Studying Plant-Bacterium Interactions
journal, September 2008
- de-Bashan, Luz E.; Bashan, Yoav
- Applied and Environmental Microbiology, Vol. 74, Issue 21
Immobilized microalgae for removing pollutants: Review of practical aspects
journal, March 2010
- de-Bashan, Luz E.; Bashan, Yoav
- Bioresource Technology, Vol. 101, Issue 6
Cultivation factors and population size control the uptake of nitrogen by the microalgae Chlorella vulgaris when interacting with the microalgae growth-promoting bacterium Azospirillum brasilense
journal, October 2005
- De-Bashan, Luz E.; Antoun, Hani; Bashan, Yoav
- FEMS Microbiology Ecology, Vol. 54, Issue 2
Increased pigment and lipid content, lipid variety, and cell and population size of the microalgae Chlorella spp. when co-immobilized in alginate beads with the microalgae-growth-promoting bacterium Azospirillum brasilense
journal, June 2002
- de-Bashan, Luz E.; Bashan, Yoav; Moreno, Manuel
- Canadian Journal of Microbiology, Vol. 48, Issue 6
Microalgae growth-promoting bacteria as “helpers” for microalgae: a novel approach for removing ammonium and phosphorus from municipal wastewater
journal, January 2004
- de-Bashan, Luz E.; Hernandez, Juan-Pablo; Morey, Taylor
- Water Research, Vol. 38, Issue 2
Removal of ammonium and phosphorus ions from synthetic wastewater by the microalgae Chlorella vulgaris coimmobilized in alginate beads with the microalgae growth-promoting bacterium Azospirillum brasilense
journal, July 2002
- de-Bashan, L.
- Water Research, Vol. 36, Issue 12
Cell-Cell Interaction in the Eukaryote-Prokaryote Model of the Microalgae Chlorella Vulgaris and the Bacterium Azospirillum Brasilense Immobilized in Polymer Beads1: Cell-Cell Interaction Between Eukaryote and Prokaryote
journal, September 2011
- de-Bashan, Luz E.; Schmid, Michael; Rothballer, Michael
- Journal of Phycology, Vol. 47, Issue 6
INVOLVEMENT OF INDOLE-3-ACETIC ACID PRODUCED BY THE GROWTH-PROMOTING BACTERIUM AZOSPIRILLUM SPP . IN PROMOTING GROWTH OF CHLORELLA VULGARIS 1
journal, August 2008
- de-Bashan, Luz E.; Antoun, Hani; Bashan, Yoav
- Journal of Phycology, Vol. 44, Issue 4
ROLE OF GLUTAMATE DEHYDROGENASE AND GLUTAMINE SYNTHETASE IN CHLORELLA VULGARIS DURING ASSIMILATION OF AMMONIUM WHEN JOINTLY IMMOBILIZED WITH THE MICROALGAE-GROWTH-PROMOTING BACTERIUM AZOSPIRILLUM BRASILENSE 1
journal, October 2008
- de-Bashan, Luz E.; Magallon, Paola; Antoun, Hani
- Journal of Phycology, Vol. 44, Issue 5
High lipid productivity of an Ankistrodesmus – Rhizobium artificial consortium
journal, October 2013
- Do Nascimento, Mauro; Dublan, Maria de los Angeles; Ortiz-Marquez, Juan Cesar Federico
- Bioresource Technology, Vol. 146
Synthetic ecology: A model system for cooperation
journal, January 2007
- Dunham, M. J.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 6
Efficiency of ammonia and phosphorus removal from a colombian agroindustrial wastewater by the microalgae Chlorella vulgaris and Scenedesmus dimorphus
journal, June 1997
- González, Luz Estela; Cañizares, Rosa Olivia; Baena, Sandra
- Bioresource Technology, Vol. 60, Issue 3
Increased Growth of the Microalga Chlorella vulgariswhen Coimmobilized and Cocultured in Alginate Beads with the Plant-Growth-Promoting Bacterium Azospirillum brasilense
journal, April 2000
- Gonzalez, Luz E.; Bashan, Yoav
- Applied and Environmental Microbiology, Vol. 66, Issue 4
Changes in the metabolism of the microalga Chlorella vulgaris when coimmobilized in alginate with the nitrogen-fixing Phyllobacterium myrsinacearum
journal, July 2000
- Gonzalez-Bashan, Luz E.; Lebsky, Vladimir K.; Hernandez, Juan P.
- Canadian Journal of Microbiology, Vol. 46, Issue 7
Environmental proteomics, biodiversity statistics and food-web structure
journal, August 2012
- Gotelli, Nicholas J.; Ellison, Aaron M.; Ballif, Bryan A.
- Trends in Ecology & Evolution, Vol. 27, Issue 8
Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes
journal, March 2005
- Gray, E. J.; Smith, D. L.
- Soil Biology and Biochemistry, Vol. 37, Issue 3
Synthetic microbial communities
journal, April 2014
- Großkopf, Tobias; Soyer, Orkun S.
- Current Opinion in Microbiology, Vol. 18
The interactions between Chlorella vulgaris and algal symbiotic bacteria under photoautotrophic and photoheterotrophic conditions
journal, October 2013
- Guo, Zhi; Tong, Yen Wah
- Journal of Applied Phycology, Vol. 26, Issue 3
A simple separation technique for purifying micro-algae
journal, June 1977
- Heaney, S. I.; Jaworski, G. H. M.
- British Phycological Journal, Vol. 12, Issue 2
Growth promotion of the freshwater microalga Chlorella vulgaris by the nitrogen-fixing, plant growth-promoting bacterium Bacillus pumilus from arid zone soils
journal, January 2009
- Hernandez, Juan-Pablo; de-Bashan, Luz E.; Rodriguez, D. Johana
- European Journal of Soil Biology, Vol. 45, Issue 1
Niche engineering demonstrates a latent capacity for fungal-algal mutualism
journal, July 2014
- Hom, Erik F. Y.; Murray, Andrew W.
- Science, Vol. 345, Issue 6192
Construction of an artificial symbiotic community using a Chlorellaâsymbiont association as a model: Construction of symbiotic association of microorganisms
journal, March 2008
- Imase, Masato; Watanabe, Keiji; Aoyagi, Hideki
- FEMS Microbiology Ecology, Vol. 63, Issue 3
Design of synthetic microbial communities for biotechnological production processes
journal, August 2014
- Jagmann, Nina; Philipp, Bodo
- Journal of Biotechnology, Vol. 184, p. 209-218
Role of Rhizobium, a plant growth promoting bacterium, in enhancing algal biomass through mutualistic interaction
journal, October 2014
- Kim, Byung-Hyuk; Ramanan, Rishiram; Cho, Dae-Hyun
- Biomass and Bioenergy, Vol. 69
Construction of bacteria–eukaryote synthetic mutualism
journal, August 2013
- Kubo, Isao; Hosoda, Kazufumi; Suzuki, Shingo
- Biosystems, Vol. 113, Issue 2
Screening and selection of growth-promoting bacteria for Dunaliella cultures
journal, July 2013
- Le Chevanton, M.; Garnier, M.; Bougaran, G.
- Algal Research, Vol. 2, Issue 3
Accumulation fatty acids of in Chlorella vulgaris under heterotrophic conditions in relation to activity of acetyl-CoA carboxylase, temperature, and co-immobilization with Azospirillum brasilense
journal, August 2014
- Leyva, Luis A.; Bashan, Yoav; Mendoza, Alberto
- Naturwissenschaften, Vol. 101, Issue 10
Artificial tripartite symbiosis involving a green alga (Chlamydomonas), a bacterium (Azotobacter) and a fungus (Alternaria): Morphological and physiological characterization
journal, July 2010
- Lőrincz, Z.; Preininger, É.; Kósa, A.
- Folia Microbiologica, Vol. 55, Issue 4
Involvement of indole-3-acetic acid produced by Azospirillum brasilense in accumulating intracellular ammonium in Chlorella vulgaris
journal, February 2015
- Meza, Beatriz; de-Bashan, Luz E.; Bashan, Yoav
- Research in Microbiology, Vol. 166, Issue 2
Accumulation of intra-cellular polyphosphate in Chlorella vulgaris cells is related to indole-3-acetic acid produced by Azospirillum brasilense
journal, June 2015
- Meza, Beatriz; de-Bashan, Luz E.; Hernandez, Juan-Pablo
- Research in Microbiology, Vol. 166, Issue 5
Using artificial systems to explore the ecology and evolution of symbioses
journal, March 2011
- Momeni, Babak; Chen, Chi-Chun; Hillesland, Kristina L.
- Cellular and Molecular Life Sciences, Vol. 68, Issue 8
Metabolic engineering of ammonium release for nitrogen-fixing multispecies microbial cell-factories
journal, May 2014
- Ortiz-Marquez, Juan Cesar Federico; Do Nascimento, Mauro; Curatti, Leonardo
- Metabolic Engineering, Vol. 23
Genetic engineering of multispecies microbial cell factories as an alternative for bioenergy production
journal, September 2013
- Ortiz-Marquez, Juan Cesar Federico; Do Nascimento, Mauro; Zehr, Jonathan Philip
- Trends in Biotechnology, Vol. 31, Issue 9
Enhancement of thiamine release during synthetic mutualism between Chlorella sorokiniana and Azospirillum brasilense growing under stress conditions
journal, August 2015
- Palacios, Oskar A.; Bashan, Yoav; Schmid, Michael
- Journal of Applied Phycology, Vol. 28, Issue 3
Synthetic microbial ecosystems for biotechnology
journal, February 2014
- Pandhal, Jagroop; Noirel, Josselin
- Biotechnology Letters, Vol. 36, Issue 6
Algal endosymbiosis in brown hydra: host/symbiont specificity
journal, December 1986
- Rahat, M.; Reich, V.
- Journal of Cell Science, Vol. 86, Issue 1
Growth and phosphorus removal by Synechococcus elongatus co-immobilized in alginate beads with Azospirillum brasilense
journal, October 2015
- Ruiz-Güereca, Duahmet Abdul; Sánchez-Saavedra, M. del Pilar
- Journal of Applied Phycology, Vol. 28, Issue 3
The Evolution of Cooperation
journal, June 2004
- Sachs, Joel L.; Mueller, Ulrich G.; Wilcox, Thomas P.
- The Quarterly Review of Biology, Vol. 79, Issue 2
Indole-3-acetic acid in microbial and microorganism-plant signaling
journal, July 2007
- Spaepen, Stijn; Vanderleyden, Jos; Remans, Roseline
- FEMS Microbiology Reviews, Vol. 31, Issue 4
Microalgal symbiosis in biotechnology
journal, May 2014
- Santos, Carla A.; Reis, Alberto
- Applied Microbiology and Biotechnology, Vol. 98, Issue 13
Evidence for a plant-associated natural habitat for Cronobacter spp.
journal, October 2009
- Schmid, Michael; Iversen, Carol; Gontia, Iti
- Research in Microbiology, Vol. 160, Issue 8
Synthetic cooperation in engineered yeast populations
journal, January 2007
- Shou, W.; Ram, S.; Vilar, J. M. G.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 6
Design and Application of New 16S rRNA-targeted Oligonucleotide Probes for the Azospirillum-Skermanella-Rhodocista-Cluster
journal, January 2001
- Stoffels, Marion; Castellanos, Thelma; Hartmann, Anton
- Systematic and Applied Microbiology, Vol. 24, Issue 1
An experimental test of the symbiosis specificity between the ciliate Paramecium bursaria and strains of the unicellular green alga Chlorella
journal, August 2007
- Summerer, Monika; Sonntag, Bettina; Sommaruga, Ruben
- Environmental Microbiology, Vol. 9, Issue 8
Symbiotic association in Chlorella culture
journal, January 2005
- Watanabe, Keiji; Takihana, Noritaka; Aoyagi, Hideki
- FEMS Microbiology Ecology, Vol. 51, Issue 2
Endosymbiosis: Lessons in Conflict Resolution
journal, March 2004
- Wernegreen, Jennifer J.
- PLoS Biology, Vol. 2, Issue 3
Emergent cooperation in microbial metabolism
journal, January 2010
- Wintermute, Edwin H.; Silver, Pamela A.
- Molecular Systems Biology, Vol. 6, Issue 1
Developing symbiotic consortia for lignocellulosic biofuel production
journal, January 2012
- Zuroff, Trevor R.; Curtis, Wayne R.
- Applied Microbiology and Biotechnology, Vol. 93, Issue 4
Works referencing / citing this record:
Azospirillum brasilense Increases CO2 Fixation on Microalgae Scenedesmus obliquus, Chlorella vulgaris, and Chlamydomonas reinhardtii Cultured on High CO2 Concentrations
journal, January 2018
- Choix, Francisco J.; López-Cisneros, Cecilia Guadalupe; Méndez-Acosta, Hugo Oscar
- Microbial Ecology, Vol. 76, Issue 2
Early Changes in Nutritional Conditions Affect Formation of Synthetic Mutualism Between Chlorella sorokiniana and the Bacterium Azospirillum brasilense
journal, November 2018
- Palacios, Oskar A.; Lopez, Blanca R.; Bashan, Yoav
- Microbial Ecology, Vol. 77, Issue 4
Azospirillum brasilense-microalga interaction increases growth and accumulation of cell compounds in Chlorella vulgaris and Tetradesmus obliquus cultured under nitrogen stress
journal, July 2019
- Ramos-Ibarra, José Roberto; Rubio-Ramírez, Tania Elizabeth; Mondragón-Cortez, Pedro
- Journal of Applied Phycology, Vol. 31, Issue 6
Enhanced performance of the microalga Chlorella sorokiniana remotely induced by the plant growth-promoting bacteria Azospirillum brasilense and Bacillus pumilus
journal, February 2017
- Amavizca, Edgar; Bashan, Yoav; Ryu, Choong-Min
- Scientific Reports, Vol. 7, Issue 1
Emerging microalgae technology: a review
journal, January 2018
- Pierobon, S. C.; Cheng, X.; Graham, P. J.
- Sustainable Energy & Fuels, Vol. 2, Issue 1
Advances in the technologies for studying consortia of bacteria and cyanobacteria/microalgae in wastewaters
journal, April 2019
- Perera, Isiri Adhiwarie; Abinandan, Sudharsanam; Subashchandrabose, Suresh R.
- Critical Reviews in Biotechnology, Vol. 39, Issue 5
Pelagibaca bermudensis promotes biofuel competence of Tetraselmis striata in a broad range of abiotic stressors: dynamics of quorum-sensing precursors and strategic improvement in lipid productivity
journal, April 2018
- Patidar, Shailesh Kumar; Kim, Sae-Hee; Kim, Jin Ho
- Biotechnology for Biofuels, Vol. 11, Issue 1
Azospirillum brasilense promotes increases in growth and nitrogen use efficiency of maize genotypes
journal, April 2019
- Zeffa, Douglas Mariani; Perini, Luiz Júnior; Silva, Mayara Barbosa
- PLOS ONE, Vol. 14, Issue 4
Maize Inoculation with Azospirillum brasilense Ab-V5 Cells Enriched with Exopolysaccharides and Polyhydroxybutyrate Results in High Productivity under Low N Fertilizer Input
journal, September 2017
- Oliveira, André L. M.; Santos, Odair J. A. P.; Marcelino, Paulo R. F.
- Frontiers in Microbiology, Vol. 8
Symbiotic Co-Culture of Scenedesmus sp. and Azospirillum brasilense on N-Deficient Media with Biomass Production for Biofuels
journal, January 2019
- Contreras-Angulo, Jose; Mata, Teresa; Cuellar-Bermudez, Sara
- Sustainability, Vol. 11, Issue 3
Combining SIMS and mechanistic modelling to reveal nutrient kinetics in an algal-bacterial mutualism
text, January 2021
- Laeverenz Schlogelhofer, Hannah; Peaudecerf, François J.; Bunbury, Freddy
- Apollo - University of Cambridge Repository
Combining SIMS and mechanistic modelling to reveal nutrient kinetics in an algal-bacterial mutualism.
text, January 2021
- Laeverenz Schlogelhofer, Hannah; Peaudecerf, François J.; Bunbury, Freddy
- Apollo - University of Cambridge Repository
Combining SIMS and mechanistic modelling to reveal nutrient kinetics in an algal-bacterial mutualism.
text, January 2021
- Laeverenz Schlogelhofer, Hannah; Peaudecerf, François J.; Bunbury, Freddy
- Apollo - University of Cambridge Repository
Correction to: Pelagibaca bermudensis promotes biofuel competence of Tetraselmis striata in a broad range of abiotic stressors: dynamics of quorum-sensing precursors and strategic improvement in lipid productivity
journal, July 2018
- Patidar, Shailesh Kumar; Kim, Sae-Hee; Kim, Jin Ho
- Biotechnology for Biofuels, Vol. 11, Issue 1
Maize Inoculation with Azospirillum brasilense Ab-V5 Cells Enriched with Exopolysaccharides and Polyhydroxybutyrate Results in High Productivity under Low N Fertilizer Input
journal, September 2017
- Oliveira, André L. M.; Santos, Odair J. A. P.; Marcelino, Paulo R. F.
- Frontiers in Microbiology, Vol. 8