Environmental parameters and microbial community profiles as indication towards microbial activities and diversity in aquaponic system compartments.
Aquaponics
Archaea
Bacteria
Chemical analysis
Community analysis
T-RFLP
Journal
BMC microbiology
ISSN: 1471-2180
Titre abrégé: BMC Microbiol
Pays: England
ID NLM: 100966981
Informations de publication
Date de publication:
06 01 2021
06 01 2021
Historique:
received:
12
06
2020
accepted:
17
12
2020
entrez:
7
1
2021
pubmed:
8
1
2021
medline:
3
11
2021
Statut:
epublish
Résumé
An aquaponic system couples cultivation of plants and fish in the same aqueous medium. The system consists of interconnected compartments for fish rearing and plant production, as well as for water filtration, with all compartments hosting diverse microbial communities, which interact within the system. Due to the design, function and operation mode of the individual compartments, each of them exhibits unique biotic and abiotic conditions. Elucidating how these conditions shape microbial communities is useful in understanding how these compartments may affect the quality of the water, in which plants and fish are cultured. We investigated the possible relationships between microbial communities from biofilms and water quality parameters in different compartments of the aquaponic system. Biofilm samples were analyzed by total community profiling for bacterial and archaeal communities. The results implied that the oxygen levels could largely explain the main differences in abiotic parameters and microbial communities in each compartment of the system. Aerobic system compartments are highly biodiverse and work mostly as a nitrifying biofilter, whereas biofilms in the anaerobic compartments contain a less diverse community. Finally, the part of the system connecting the aerobic and anaerobic processes showed common conditions where both aerobic and anaerobic processes were observed. Different predicted microbial activities for each compartment were found to be supported by the abiotic parameters, of which the oxygen saturation, total organic carbon and total nitrogen differentiated clearly between samples from the main aerobic loop and the anaerobic compartments. The latter was also confirmed using microbial community profile analysis.
Sections du résumé
BACKGROUND
An aquaponic system couples cultivation of plants and fish in the same aqueous medium. The system consists of interconnected compartments for fish rearing and plant production, as well as for water filtration, with all compartments hosting diverse microbial communities, which interact within the system. Due to the design, function and operation mode of the individual compartments, each of them exhibits unique biotic and abiotic conditions. Elucidating how these conditions shape microbial communities is useful in understanding how these compartments may affect the quality of the water, in which plants and fish are cultured.
RESULTS
We investigated the possible relationships between microbial communities from biofilms and water quality parameters in different compartments of the aquaponic system. Biofilm samples were analyzed by total community profiling for bacterial and archaeal communities. The results implied that the oxygen levels could largely explain the main differences in abiotic parameters and microbial communities in each compartment of the system. Aerobic system compartments are highly biodiverse and work mostly as a nitrifying biofilter, whereas biofilms in the anaerobic compartments contain a less diverse community. Finally, the part of the system connecting the aerobic and anaerobic processes showed common conditions where both aerobic and anaerobic processes were observed.
CONCLUSION
Different predicted microbial activities for each compartment were found to be supported by the abiotic parameters, of which the oxygen saturation, total organic carbon and total nitrogen differentiated clearly between samples from the main aerobic loop and the anaerobic compartments. The latter was also confirmed using microbial community profile analysis.
Identifiants
pubmed: 33407126
doi: 10.1186/s12866-020-02075-0
pii: 10.1186/s12866-020-02075-0
pmc: PMC7789318
doi:
Substances chimiques
Carbon
7440-44-0
Nitrogen
N762921K75
Oxygen
S88TT14065
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
12Subventions
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
ID : 310030_169665
Références
Branda SS, Vik Å, Friedman L, Kolter R. Biofilms: the matrix revisited. Trends Microbiol. 2005;13:20–6.
pubmed: 15639628
doi: 10.1016/j.tim.2004.11.006
pmcid: 15639628
Davey ME, O’Toole GA. Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev. 2000;64:847–67.
pubmed: 11104821
pmcid: 99016
doi: 10.1128/MMBR.64.4.847-867.2000
Donlan RM. Biofilms: microbial life on surfaces. Emerg Infect Dis. 2002;8:881–90.
pubmed: 12194761
pmcid: 2732559
doi: 10.3201/eid0809.020063
Timmons MB, Ebeling JM. Recirculating aquaculture. Cayuga Aqua Ventures: Ithaca, United States; 2010.
Ebeling JM, Timmons MB, Bisogni JJ. Engineering analysis of the stoichiometry of photoautotrophic, autotrophic, and heterotrophic removal of ammonia–nitrogen in aquaculture systems. Aquaculture. 2006;257:346–58.
doi: 10.1016/j.aquaculture.2006.03.019
Schmautz Z, Graber A, Jaenicke S, Goesmann A, Junge R, Smits THM. Microbial diversity in different compartments of an aquaponics system. Arch Microbiol. 2017;199:613–20.
pubmed: 28074233
doi: 10.1007/s00203-016-1334-1
pmcid: 28074233
Somerville C, Cohen M, Pantanella E, Stankus A, Lovatelli A. Small-scale aquaponic food production: integrated fish and plant farming. FAO Fisheries and Aquaculture Technical Paper Food and Agriculture Organization of the United Nations: Rome, Italy; 2014.
Rakocy JE, Masser MP, Losordo TM. Recirculating aquaculture tank production systems: Aquaponics-integrating fish and plant culture. SRAC Publ. 2006;454.
Xu J, Liu Y, Cui S, Miao X. Behavioral responses of tilapia (Oreochromis niloticus) to acute fluctuations in dissolved oxygen levels as monitored by computer vision. Aquac Eng. 2006;35:207–17.
doi: 10.1016/j.aquaeng.2006.02.004
El-Sayed A-FM, Kawanna M. Optimum water temperature boosts the growth performance of Nile tilapia (Oreochromis niloticus) fry reared in a recycling system. Aquac Res. 2008;39:670–2.
doi: 10.1111/j.1365-2109.2008.01915.x
Makri O, Kintzios S. Ocimum sp. (basil): botany, cultivation, pharmaceutical properties, and biotechnology. Int J Geogr Inf Syst. 2008;13:123–50.
Graber A, Junge R. Aquaponic systems: nutrient recycling from fish wastewater by vegetable production. Desalination. 2009;246:147–56.
doi: 10.1016/j.desal.2008.03.048
Vergot N, Vermeulen J. Recirculation aquaculture system (RAS) with tilapia in a hydroponic system with tomatoes. Acta Hortic. 2012;927:67–74.
König B, Janker J, Reinhardt T, Villarroel M, Junge R. Analysis of aquaponics as an emerging technological innovation system. J Clean Prod. 2018;180:232–43.
doi: 10.1016/j.jclepro.2018.01.037
Boyd CE. Water quality: an introduction. 2nd ed: Springer; 2015.
Kowalchuk GA, Stephen JR. Ammonia-oxidizing bacteria: A model for molecular microbial ecology. Annu Rev Microbiol. 2001;55:485–529.
pubmed: 11544365
doi: 10.1146/annurev.micro.55.1.485
pmcid: 11544365
Jørgensen NOG. Organic Nitrogen. In: Likens GE (ed) Encyclopedia of Inland Waters. Academic Press, Elsevier Inc.; 2009. p. 832–51.
Barker AV, Pilbeam DJ. Handbook of plant nutrition. 2nd ed: CRC Press; 2015. https://doi.org/10.1201/b18458 .
Prairie YT. Carbocentric limnology: looking back, looking forward. Can J Fish Aquat Sci. 2008;65:543–8.
doi: 10.1139/f08-011
Seekell DA, Lapierre J-F, Cheruvelil KS. A geography of lake carbon cycling. Limnol Oceanogr Lett. 2018;3:49–56.
doi: 10.1002/lol2.10078
Eck M, Sare AR, Massart S, Schmautz Z, Junge R, Smits THM, et al. Exploring bacterial communities in aquaponic systems. Water. 2019;11:260.
doi: 10.3390/w11020260
Tyson RV, Simonne EH, Treadwell DD, White JM, Simonne A. Reconciling pH for ammonia biofiltration and cucumber yield in a recirculating aquaponic system with perlite biofilters. HortScience. 2008;43:719–24.
doi: 10.21273/HORTSCI.43.3.719
Berendsen RL, Pieterse CMJ, Bakker PAHM. The rhizosphere microbiome and plant health. Trends Plant Sci. 2012;17:478–86.
pubmed: 22564542
pmcid: 22564542
doi: 10.1016/j.tplants.2012.04.001
Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P. Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol. 2013;64:807–38.
pubmed: 23373698
pmcid: 23373698
doi: 10.1146/annurev-arplant-050312-120106
Al-Dawery SK. Conditioning process and characterization of fresh activated sludge. Int J Eng Sci Technol. 2015;10:692–711.
Endut A, Jusoh A, Ali N. Nitrogen budget and effluent nitrogen components in aquaponics recirculation system. Desalination Water Treat. 2014;52:744–52.
doi: 10.1080/19443994.2013.826336
Maathuis FJ. Physiological functions of mineral macronutrients. Curr Opin Plant Biol. 2009;12:250–8.
pubmed: 19473870
doi: 10.1016/j.pbi.2009.04.003
pmcid: 19473870
Søndergaard M. Redox potential. In: Encyclopedia of inland waters. Oxford: Academic Press; 2009. p. 852–9. https://doi.org/10.1016/B978-012370626-3.00115-0 .
doi: 10.1016/B978-012370626-3.00115-0
Hirano S, Matsumoto N, Morita M, Sasaki K, Ohmura N. Electrochemical control of redox potential affects methanogenesis of the hydrogenotrophic methanogen Methanothermobacter thermautotrophicus. Lett Appl Microbiol. 2013;56:315–21.
pubmed: 23413966
doi: 10.1111/lam.12059
pmcid: 23413966
Tokarz E, Urban D. Soil redox potential and its impact on microorganisms and plants of wetlands. J Ecol Eng. 2015;16:20–30.
doi: 10.12911/22998993/2801
Christensen TH, Bjerg PL, Banwart SA, Jakobsen R, Heron G, Albrechtsen H-J. Characterization of redox conditions in groundwater contaminant plumes. J Contam Hydrol. 2000;45:165–241.
doi: 10.1016/S0169-7722(00)00109-1
van Rijn J, Tal Y, Schreier HJ. Denitrification in recirculating systems: theory and applications. Aquac Eng. 2006;34:364–76.
doi: 10.1016/j.aquaeng.2005.04.004
Wongkiew S, Hu Z, Chandran K, Lee JW, Khanal SK. Nitrogen transformations in aquaponic systems: a review. Aquac Eng. 2017;76:9–19.
doi: 10.1016/j.aquaeng.2017.01.004
Robertson GP, Groffman PM. Nitrogen transformations. In: Paul EA, editor. Soil microbiology, biochemistry, and ecology. 3rd ed. New York: Springer; 2007. p. 341–64. https://doi.org/10.1016/B978-0-08-047514-1.50017-2 .
doi: 10.1016/B978-0-08-047514-1.50017-2
Hagemann N, Harter J, Behrens S. Elucidating the impacts of biochar applications on nitrogen cycling microbial communities. In: Ralebitso-Senior TK, H. Orr C, editors. Biochar Application. Elsevier; 2016. p. 163–198. doi: https://doi.org/10.1016/B978-0-12-803433-0.00007-2 .
Errebhi M, Wilcox GE. Plant species response to ammonium-nitrate concentration ratios. J Plant Nutr. 1990;13:1017–29.
doi: 10.1080/01904169009364132
Osborn AM, Moore ERB, Timmis KN. An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environ Microbiol. 2000;2:39–50.
pubmed: 11243261
doi: 10.1046/j.1462-2920.2000.00081.x
pmcid: 11243261
Wanner J. Activated sludge population dynamics. Water Sci Technol Lond. 1994;30:159–69.
doi: 10.2166/wst.1994.0556
Bartelme RP, Smith MC, Sepulveda-Villet OJ, Newton RJ. Component microenvironments and system biogeography structure microorganism distributions in recirculating aquaculture and aquaponic systems. mSphere. 2019;4:e00143–19.
pubmed: 31270175
pmcid: 6609224
doi: 10.1128/mSphere.00143-19
Blackwood CB, Hudleston D, Zak DR, Buyer JS. Interpreting ecological diversity indices applied to terminal restriction fragment length polymorphism data: insights from simulated microbial communities. Appl Environ Microbiol. 2007;73:5276–83.
pubmed: 17601815
pmcid: 1950973
doi: 10.1128/AEM.00514-07
Dickie IA, FitzJohn RG. Using terminal restriction fragment length polymorphism (T-RFLP) to identify mycorrhizal fungi: a methods review. Mycorrhiza. 2007;17:259–70.
pubmed: 17429700
doi: 10.1007/s00572-007-0129-2
pmcid: 17429700
Bartelme RP, McLellan SL, Newton RJ. Freshwater recirculating aquaculture system operations drive biofilter bacterial community shifts around a stable nitrifying consortium of ammonia-oxidizing archaea and COMAMMOX Nitrospira. Front Microbiol. 2017;8:101.
pubmed: 28194147
pmcid: 5276851
doi: 10.3389/fmicb.2017.00101
Stein LY, Klotz MG. The nitrogen cycle. Curr Biol. 2016;26:R94–8.
pubmed: 26859274
doi: 10.1016/j.cub.2015.12.021
pmcid: 26859274
Francis CA, Beman JM, Kuypers MMM. New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J. 2007;1:19–27.
pubmed: 18043610
doi: 10.1038/ismej.2007.8
pmcid: 18043610
Fernandez D. HydroBuddy: an open source nutrient calculator for hydroponics and general agriculture. 2016. http://scienceinhydroponics.com .
Culman SW, Bukowski R, Gauch HG, Cadillo-Quiroz H, Buckley DH. T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinformatics. 2009;10:171.
pubmed: 19500385
pmcid: 2702334
doi: 10.1186/1471-2105-10-171
Hammer Ø, Harper DAT, Ryan PD. PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron. 2001;4:4–9.
R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R foundation for statistical computing; 2018. https://www.R-project.org/ .
de Mendiburu F. agricolae: Statistical procedures for agricultural research. 2019. https://CRAN.R-project.org/package=agricolae .
Wickham H, Hester J, Chang W. devtools: Tools to make developing R packages easier. 2019. https://CRAN.R-project.org/package=devtools .
Wickham H, François R, Henry L, Müller K. dplyr: A grammar of data manipulation. 2019. https://CRAN.R-project.org/package=dplyr .
Vu VQ. ggbiplot: A ggplot2 based biplot. 2011. http://github.com/vqv/ggbiplot .
Kassambara A. ggpubr: “ggplot2” based publication ready plots. 2019. https://CRAN.R-project.org/package=ggpubr .
Komsta L, Novomestky F. moments: Moments, cumulants, skewness, kurtosis and related tests. 2015. https://CRAN.R-project.org/package=moments .
Wickham H. scales: Scale functions for visualization. 2018. https://CRAN.R-project.org/package=scales .
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: Community ecology package. 2019. https://CRAN.R-project.org/package=vegan .
Shannon CE. A mathematical theory of communication. Bell Syst Tech J. 1948;27:379–423.
doi: 10.1002/j.1538-7305.1948.tb01338.x
Simpson EH. Measurement of diversity. Nature. 1949;163:688.
doi: 10.1038/163688a0