The importance of several factors that drive the symbiotic interactions between bacteria and microalgae in consortia has been well realised. However, the implication of extracellular polymeric substances (EPS) released by the partners remains unclear. Therefore, the present study focused on the influence of EPS in developing consortia of a bacterium, Variovorax paradoxus IS1, with a microalga, Tetradesmus obliquus IS2 or Coelastrella sp. IS3, all isolated from poultry slaughterhouse wastewater. The bacterium increased the specific growth rates of microalgal species significantly in the consortia by enhancing the uptake of nitrate (88‒99%) and phosphate (92‒95%) besides accumulating higher amounts of carbohydrates and proteins. The EPS obtained from exudates, collected from the bacterial or microalgal cultures, contained numerous phytohormones, vitamins, polysaccharides and amino acids that are likely involved in interspecies interactions. The addition of EPS obtained from V. paradoxus IS1 to the culture medium doubled the growth of both the microalgal strains. The EPS collected from T. obliquus IS2 significantly increased the growth of V. paradoxus IS1, but there was no apparent change in bacterial growth when it was cultured in the presence of EPS from Coelastrella sp. IS3. These observations indicate that the interaction between V. paradoxus IS1 and T. obliquus IS2 was mutualism, while commensalism was the interaction between the bacterial strain and Coelastrella sp. IS3. Our present findings thus, for the first time, unveil the EPS-induced symbiotic interactions among the partners involved in bacterial‒microalgal consortia.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Subashchandrabose SR, Ramakrishnan B, Megharaj M, Naidu R (2011) Consortia of cyanobacteria/microalgae and bacteria: biotechnological potential. Biotechnol Adv 29:896–907. https://doi.org/10.1016/j.biotechadv.2011.07.009
García D, de Godos I, Domínguez C, Turiel S, Bolado S, Muñoz R (2019) A systematic comparison of the potential of microalgae-bacteria and purple phototrophic bacteria consortia for the treatment of piggery wastewater. Bioresour Technol 276:18–27. https://doi.org/10.1016/j.biortech.2018.12.095
Peng H, de Bashan LE, Bashan Y, Higgins BT (2020) Indole-3-acetic acid from Azosprillum brasilense promotes growth in green algae at the expense of energy storage products. Algal Res 47:101845. https://doi.org/10.1016/j.algal.2020.101845
Abinandan S, Subashchandrabose SR, Venkateswarlu K, Megharaj M (2018) Microalgae–bacteria biofilms: a sustainable synergistic approach in remediation of acid mine drainage. Appl Microbiol Biotechnol 102:1131–1144. https://doi.org/10.1007/s00253-017-8693-7
Perera I, Subashchandrabose SR, Venkateswarlu K, Naidu R, Megharaj M (2018) Consortia of cyanobacteria/microalgae and bacteria in desert soils: an underexplored microbiota. Appl Microbiol Biotechnol 102:7351–7363. https://doi.org/10.1007/s00253-018-9192-1
Perera IA, Abinandan S, Subashchandrabose SR, Venkateswarlu K, Naidu R, Megharaj M (2019) Advances in the technologies for studying consortia of bacteria and cyanobacteria/microalgae in wastewaters. Crit Rev Biotechnol 39:709–731. https://doi.org/10.1080/07388551.2019.1597828
Higgins BT, Labavitch JM, VanderGheynst JS (2015) Co-culturing Chlorella minutissima with Escherichia coli can increase neutral lipid production and improve biodiesel quality. Biotechnol Bioeng 112:1801–1809. https://doi.org/10.1002/bit.25609
Higgins BT, Gennity I, Fitzgerald PS, Ceballos SJ, Fiehn O, VanderGheynst JS (2018) Algal–bacterial synergy in treatment of winery wastewater. npj Clean Water 1:6. https://doi.org/10.1038/s41545-018-0005-y
Abinandan S, Subashchandrabose SR, Venkateswarlu K, Megharaj M (2018) Nutrient removal and biomass production: advances in microalgal biotechnology for wastewater treatment. Crit Rev Biotechnol 38:1244–1260. https://doi.org/10.1080/07388551.2018.1472066
Palacios OA, Gomez-Anduro G, Bashan Y, de Bashan LE (2016) Tryptophan, thiamine and indole-3-acetic acid exchange between Chlorella sorokiniana and the plant growth-promoting bacterium Azospirillum brasilense. FEMS Microbiol Ecol 92:fiw077. https://doi.org/10.1093/femsec/fiw077
Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438:90–93. https://doi.org/10.1038/nature04056
Grant MAA, Kazamia E, Cicuta P, Smith AG (2014) Direct exchange of vitamin B12 is demonstrated by modelling the growth dynamics of algal–bacterial co-cultures. ISME J 8:1418–1427. https://doi.org/10.1038/ismej.2014.9
Cooper MB, Kazamia E, Helliwell KE, Kudahl UJ, Sayer A, Wheeler GL, Smith AG (2019) Cross-exchange of B-vitamins underpins a mutualistic interaction between Ostreococcus tauri and Dinoroseobacter shibae. ISME J 13:334–345. https://doi.org/10.1038/s41396-018-0274-y
Taylor JD, McKew BA, Kuhl A, McGenity TJ, Underwood GJC (2013) Microphytobenthic extracellular polymeric substances (EPS) in intertidal sediments fuel both generalist and specialist EPS-degrading bacteria. Limnol Oceanogr 58:1463–1480. https://doi.org/10.4319/lo.2013.58.4.1463
Wei Z, Huang S, Zhang Y, Li H, Zhou S (2017) Characterisation of extracellular polymeric substances produced during nitrate removal by a thermophilic bacterium Chelatococcus daeguensis TAD1 in batch cultures. RSC Adv 7:44265–44271. https://doi.org/10.1039/C7RA08147B
Rusanowska P, Cydzik-Kwiatkowska A, Wojnowska-Baryła I (2019) Microbial origin of excreted DNA in particular fractions of extracellular polymers (EPS) in aerobic granules. Water Air Soil Pollut 230:203. https://doi.org/10.1007/s11270-019-4248-0
Xiao R, Yang X, Li M, Li X, Wei Y, Cao M, Ragauskas A, Thies M, Ding J, Zheng Y (2018) Investigation of composition, structure and bioactivity of extracellular polymeric substances from original and stress-induced strains of Thraustochytrium striatum. Carbohydr Polym 195:515–524. https://doi.org/10.1016/j.carbpol.2018.04.126
Jiao Y, Cody GD, Harding AK, Wilmes P, Schrenk M, Wheeler KE, Banfield JF, Thelen MP (2010) Characterisation of extracellular polymeric substances from acidophilic microbial biofilms. Appl Environ Microbiol 76:2916–2922. https://doi.org/10.1128/AEM.02289-09
Cao B, Shi L, Brown RN, Xiong Y, Fredrickson JK, Romine MF, Marshall MJ, Lipton MS, Beyenal H (2011) Extracellular polymeric substances from Shewanella sp. HRCR-1 biofilms: characterisation by infrared spectroscopy and proteomics. Environ Microbiol 13:1018–1031. https://doi.org/10.1111/j.1462-2920.2010.02407.x
Perera IA, Abinandan S, Subashchandrabose SR, Venkateswarlu K, Naidu R, Megharaj M (2021) Microalgal–bacterial consortia unveil distinct physiological changes to facilitate growth of microalgae. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiab012
Peniuk GT, Schnurr PJ, Allen DG (2016) Identification and quantification of suspended algae and bacteria populations using flow cytometry: applications for algae biofuel and biochemical growth systems. J Appl Phycol 28:95–104. https://doi.org/10.1007/s10811-015-0569-6
Abinandan S, Subashchandrabose SR, Venkateswarlu K, Megharaj M (2020) Sustainable iron recovery and biodiesel yield by acid-adapted microalgae, Desmodesmus sp. MAS1 and Heterochlorella sp. MAS3, grown in synthetic acid mine drainage. ACS Omega 5:6888–6894. https://doi.org/10.1021/acsomega.0c00255
Rice EW, Baird RB, Eaton AD, Clesceri LS (2012) Standard methods for the examination of water and wastewater. Washington DC: American Public Health Association
Zhang R, Neu TR, Li Q, Blanchard V, Zhang Y, Schippers A, Sand W (2019) Insight into interactions of thermoacidophilic archaea with elemental sulfur: biofilm dynamics and EPS analysis. Front Microbiol 10:896. https://doi.org/10.3389/fmicb.2019.00896
Kim HK, Choi YH, Verpoorte R (2010) NMR-based metabolomic analysis of plants. Nat Protoc 5:536–549. https://doi.org/10.1038/nprot.2009.237
Gonzalez-Gil G, Thomas L, Emwas A-H, Lens PNL, Saikaly PE (2015) NMR and MALDI-TOF MS based characterisation of exopolysaccharides in anaerobic microbial aggregates from full-scale reactors. Sci Rep 5:14316. https://doi.org/10.1038/srep14316
Chong J, Soufan O, Li C, Caraus I, Li S, Bourque G, Wishart DS, Xia J (2018) MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res 46:W486–W494. https://doi.org/10.1093/nar/gky310
Cui H, Yang S-S, Pang J-W, Mi H-R, Nuer C-C, Ding J (2020) An improved ASM-GDA approach to evaluate the production kinetics of loosely bound and tightly bound extracellular polymeric substances in biological phosphorus removal process. RSC Adv 10:2495–2506. https://doi.org/10.1039/C9RA06845G
Abinandan S, Subashchandrabose SR, Venkateswarlu K, Perera IA, Megharaj M (2019) Acid-tolerant microalgae can withstand higher concentrations of invasive cadmium and produce sustainable biomass and biodiesel at pH 3.5. Bioresour Technol 281:469–473. https://doi.org/10.1016/j.biortech.2019.03.001
Khan MSI, Lee E-J, Kim Y-J (2016) A submerged dielectric barrier discharge plasma inactivation mechanism of biofilms produced by Escherichia coli O157:H7, Cronobacter sakazakii, and Staphylococcus aureus. Sci Rep 6:37072. https://doi.org/10.1038/srep37072
Kumar M, Kumar M, Pandey A, Thakur IS (2019) Genomic analysis of carbon dioxide sequestering bacterium for exopolysaccharides production. Sci Rep 9:4270. https://doi.org/10.1038/s41598-019-41052-0
Mishra A, Kavita K, Jha B (2011) Characterisation of extracellular polymeric substances produced by micro-algae Dunaliella salina. Carbohydr Polym 83:852–857. https://doi.org/10.1016/j.carbpol.2010.08.067
Goecke F, Thiel V, Wiese J, Labes A, Imhoff JF (2013) Algae as an important environment for bacteria–phylogenetic relationships among new bacterial species isolated from algae. Phycologia 52:14–24. https://doi.org/10.2216/12-24.1
Carreres BM, León-Saiki GM, Schaap PJ, Remmers IM, van der Veen D, Martins dos Santos VAP, Wijffels RH, Martens DE, Suarez-Diez M (2019) The diurnal transcriptional landscape of the microalga Tetradesmus obliquus. Algal Res 40:101477. https://doi.org/10.1016/j.algal.2019.101477
Mujtaba G, Rizwan M, Lee K (2017) Removal of nutrients and COD from wastewater using symbiotic co-culture of bacterium Pseudomonas putida and immobilised microalga Chlorella vulgaris. J Indust Eng Chem 49:145–151. https://doi.org/10.1016/j.jiec.2017.01.021
Ji X, Jiang M, Zhang J, Jiang X, Zheng Z (2018) The interactions of algae-bacteria symbiotic system and its effects on nutrients removal from synthetic wastewater. Bioresour Technol 247:44–50. https://doi.org/10.1016/j.biortech.2017.09.074
Ji X, Li H, Zhang J, Saiyin H, Zheng Z (2019) The collaborative effect of Chlorella vulgaris-Bacillus licheniformis consortia on the treatment of municipal water. J Hazard Mater 365:483–493. https://doi.org/10.1016/j.jhazmat.2018.11.039
Ferro L, Colombo M, Posadas E, Funk C, Muñoz R (2019) Elucidating the symbiotic interactions between a locally isolated microalga Chlorella vulgaris and its co-occurring bacterium Rhizobium sp. in synthetic municipal wastewater. J Appl Phycol 31:2299–2310. https://doi.org/10.1007/s10811-019-1741-1
Yang L, Chen J, Qin S, Zeng M, Jiang Y, Hu L, Xiao P, Hao W, Hu Z, Lei A, Wang J (2018) Growth and lipid accumulation by different nutrients in the microalga Chlamydomonas reinhardtii. Biotechnol Biofuels 11:40–40. https://doi.org/10.1186/s13068-018-1041-z
Xie T, Xia Y, Zeng Y, Li X, Zhang Y (2017) Nitrate concentration-shift cultivation to enhance protein content of heterotrophic microalga Chlorella vulgaris: over-compensation strategy. Bioresour Technol 233:247–255. https://doi.org/10.1016/j.biortech.2017.02.099
Okazaki H, Takabe Y, Masuda T, Hoshikawa Y (2019) Biochemical response of indigenous microalgal consortia to variations in nitrogen concentration of treated effluent. Bioresour Technol 280:118–126. https://doi.org/10.1016/j.biortech.2019.02.014
Camacho F, Macedo A, Malcata F (2019) Potential industrial applications and commercialisation of microalgae in the functional food and feed industries: a short review. Mar Drugs 17:312. https://doi.org/10.3390/md17060312
Liu L, Pohnert G, Wei D (2016) Extracellular metabolites from industrial microalgae and their biotechnological potential. Mar Drugs 14:191. https://doi.org/10.3390/md14100191
Ferrer-González FX, Widner B, Holderman NR, Glushka J, Edison AS, Kujawinski EB, Moran MA (2020) Resource partitioning of phytoplankton metabolites that support bacterial heterotrophy. ISME J 14:1369–1383. https://doi.org/10.1038/s41396-020-00811-y
Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448. https://doi.org/10.1111/j.1574-6976.2007.00072.x
Wang D, Ding X, Rather PN (2001) Indole can cct as an extracellular signal in Escherichia coli. J Bacteriol 183:4210–4216. https://doi.org/10.1128/JB.183.14.4210-4216.2001
Palacios OA, Lopez BR, Bashan Y, de Bashan LE (2019) Early changes in nutritional conditions affect formation of synthetic mutualism between Chlorella sorokiniana and the bacterium Azospirillum brasilense. Microb Ecol 77:980–992. https://doi.org/10.1007/s00248-018-1282-1
Schauer K, Stolz J, Scherer S, Fuchs TM (2009) Both Thiamine uptake and biosynthesis of thiamine precursors are required for intracellular replication of Listeria monocytogenes. J Bacteriol 191:2218–2227. https://doi.org/10.1128/JB.01636-08
Rosenberg J, Ischebeck T, Commichau FM (2017) Vitamin B6 metabolism in microbes and approaches for fermentative production. Biotechnol Adv 35:31–40. https://doi.org/10.1016/j.biotechadv.2016.11.004
Palacios OA, Choix FJ, Bashan Y, de Bashan LE (2016) Influence of tryptophan and indole-3-acetic acid on starch accumulation in the synthetic mutualistic Chlorella sorokiniana–Azospirillum brasilense system under heterotrophic conditions. Res Microbiol 167:367–379. https://doi.org/10.1016/j.biotechadv.2016.11.004
Segev E, Wyche TP, Kim KH, Petersen J, Ellebrandt C, Valamakis H, Barteneva N, Paulson JN, Chai L, Clardy J, Kolter R (2016) Dynamic metabolic exchange governs a marine algal-bacterial interaction. Elife 5:e17473. https://doi.org/10.7554/eLife.17473
IP acknowledges the University of Newcastle for UNRS and UNIPRS scholarships, and SRS acknowledges the University of Newcastle for ECR HDR scholarship and CRC CARE.
Conflict of Interest
The authors declare no competing interests.
Below is the link to the electronic supplementary material.
About this article
Cite this article
Perera, I.A., Abinandan, S., Subashchandrabose, S.R. et al. Extracellular Polymeric Substances Drive Symbiotic Interactions in Bacterial‒Microalgal Consortia. Microb Ecol (2021). https://doi.org/10.1007/s00248-021-01772-1
- Bacterial‒microalgal consortia
- Extracellular polymeric substances
- Symbiotic interactions
- Nutrient uptake