{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,12]],"date-time":"2026-08-12T17:08:31Z","timestamp":1786554511752,"version":"build-2736575974"},"reference-count":55,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2020,12,11]],"date-time":"2020-12-11T00:00:00Z","timestamp":1607644800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Bioeng. Biotechnol."],"abstract":"<jats:p>In order to effectively use microbial-based strategies to manage anaerobic digesters, it is necessary to distinguish between community shifts that are part of the natural dynamic of the system and shifts caused by environmental or operational disturbances. The objective of this research study was to evaluate the significance of changes in the microbial community of anaerobic digesters during failure in correlation to operational parameters such as an organic acid overload. Five continuously stirred 0.5 L reactors were set-up as semi-continuously-fed, mesophilic dairy manure digesters with a 30-day hydraulic retention time. After a 120-day stabilization period, two digesters were kept as controls, while the organic loading rates in the triplicate set were increased step-wise to ultimately provide a shock-load leading to failure using propionic acid spikes. Acidosis resulting in near cessation of biogas and termination of methane production occurred between 4 and 7 weeks, after which all the digesters continued to be fed only dairy manure. The shock loading of propionic acid led to an accumulation of mainly acetate and propionate, with low levels of iso-butyrate, butyrate, iso-valerate, and valerate. High-throughput Illumina sequencing of the V4 region of the bacterial and archaeal 16S rRNA gene in digester samples showed a significant change in the microbial community composition during propionic acid overload, followed by a return to the original composition with regular feedstock. Bacterial genera whose relative abundance decreased during the inhibition stage included <jats:italic>Sedimentibacter<\/jats:italic>, <jats:italic>Syntrophomonas<\/jats:italic>, <jats:italic>TSCOR003.O20<\/jats:italic>, and Marinilabiaceae, while the relative abundance of Lachnospiraceae, <jats:italic>Ruminococcus<\/jats:italic>, Mogibacteriaceae, <jats:italic>Pyramidobacter<\/jats:italic>, and <jats:italic>Bacteroides<\/jats:italic> increased. The relative abundance of dominant methanogens, <jats:italic>Methanosarcina<\/jats:italic> and <jats:italic>Methanobacterium<\/jats:italic>, although initially resistant, were decreased (from 91.71 to 12.14% and from 2.98 to 0.73%, respectively) during inhibition, while <jats:italic>Methanobrevibacter<\/jats:italic> and <jats:italic>Methanosphaera<\/jats:italic> that were prominent in the manure feedstock increased from 17.36 to 79.45% and from 0.14 to 1.12%, respectively. Shifts in bacterial and archaeal compositions, back to their pre-shock steady state after failure, highlight the digester\u2019s microbial resilience and recovery potential.<\/jats:p>","DOI":"10.3389\/fbioe.2020.604838","type":"journal-article","created":{"date-parts":[[2020,12,11]],"date-time":"2020-12-11T08:05:22Z","timestamp":1607673922000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":46,"title":["Response of Microbial Community to Induced Failure of Anaerobic Digesters Through Overloading With Propionic Acid Followed by Process Recovery"],"prefix":"10.3389","volume":"8","author":[{"given":"Azin","family":"Khafipour","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elsie M.","family":"Jordaan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel","family":"Flores-Orozco","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ehsan","family":"Khafipour","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David B.","family":"Levin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard","family":"Sparling","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nazim","family":"Cicek","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2020,12,11]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1007\/BF00218466","article-title":"Volatile fatty acids as indicators of process imbalance in anaerobic digestors.","volume":"43","author":"Ahring","year":"1995","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"B2","author":"Anderson","year":"2005","journal-title":"PERMANOVA-Permutational Multivariate Analysis of Variance."},{"key":"B3","author":"Eaton","year":"1995","journal-title":"Standard Methods"},{"key":"B4","doi-asserted-by":"publisher","first-page":"2129","DOI":"10.1007\/s12010-013-0465-y","article-title":"Quantitative analysis of previously identified propionate-oxidizing bacteria and methanogens at different temperatures in an UASB reactor containing propionate as a sole carbon source.","volume":"171","author":"Ban","year":"2013","journal-title":"Appl. Biochem. Biotechnol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1038\/nmeth.f.303","article-title":"QIIME allows analysis of high-throughput community sequencing data.","volume":"7","author":"Caporaso","year":"2010","journal-title":"Nat. Methods"},{"key":"B6","doi-asserted-by":"publisher","first-page":"1621","DOI":"10.1038\/ismej.2012.8","article-title":"Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms.","volume":"6","author":"Caporaso","year":"2012","journal-title":"ISME J."},{"key":"B7","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1016\/j.copbio.2015.01.008","article-title":"Microbial management of anaerobic digestion: exploiting the microbiome-functionality nexus.","volume":"33","author":"Carballa","year":"2015","journal-title":"Curr. Opin. Biotechnol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"519","DOI":"10.1016\/j.chemosphere.2015.12.003","article-title":"Proteolytic bacterial dominance in a full-scale municipal solid waste anaerobic reactor assessed by 454 pyrosequencing technology.","volume":"146","author":"Cardinali-Rezende","year":"2016","journal-title":"Chemosphere"},{"key":"B9","doi-asserted-by":"publisher","first-page":"1371","DOI":"10.1111\/jam.12001","article-title":"Impact of substrate overloading on archaeal populations in anaerobic digestion of animal waste.","volume":"113","author":"Chen","year":"2012","journal-title":"J. Appl. Microbiol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"2153","DOI":"10.1080\/09593330.2016.1247197","article-title":"Metagenomic analysis and performance of a mesophilic anaerobic reactor treating food waste at various load rates.","volume":"38","author":"da Silva Martins","year":"2017","journal-title":"Environ. Technol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1016\/j.biortech.2014.10.126","article-title":"Microbial diversity and dynamicity of biogas reactors due to radical changes of feedstock composition.","volume":"176","author":"De Francisci","year":"2015","journal-title":"Bioresour. Technol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"5069","DOI":"10.1128\/AEM.03006-05","article-title":"Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB.","volume":"72","author":"DeSantis","year":"2006","journal-title":"Appl. Environ. Microbiol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.biortech.2012.02.079","article-title":"Methanosarcina: the rediscovered methanogen for heavy duty biomethanation.","volume":"112","author":"De Vrieze","year":"2012","journal-title":"Bioresour. Technol."},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2016.00426","article-title":"The features of fecal and ileal mucosa-associated microbiota in dairy calves during early infection with Mycobacterium avium subspecies paratuberculosis.","volume":"7","author":"Derakhshani","year":"","journal-title":"Front. Microbiol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"321","DOI":"10.1002\/jobm.201500420","article-title":"An extended single-index multiplexed 16S rRNA sequencing for microbial community analysis on MiSeq illumina platforms.","volume":"56","author":"Derakhshani","year":"","journal-title":"J. Basic Microbiol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"4942","DOI":"10.1128\/AEM.02985-05","article-title":"Phenotypic properties and microbial diversity of methanogenic granules from a full-scale upflow anaerobic sludge bed reactor treating brewery wastewater.","volume":"72","author":"Diaz","year":"2006","journal-title":"Appl. Environ. Microbiol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"2460","DOI":"10.1093\/bioinformatics\/btq461","article-title":"Search and clustering orders of magnitude faster than BLAST.","volume":"26","author":"Edgar","year":"2010","journal-title":"Bioinformatics"},{"key":"B18","doi-asserted-by":"publisher","first-page":"2194","DOI":"10.1093\/bioinformatics\/btr381","article-title":"UCHIME improves sensitivity and speed of chimera detection.","volume":"27","author":"Edgar","year":"2011","journal-title":"Bioinformatics"},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.1016\/j.biortech.2020.123889","article-title":"Effect of mesophilic anaerobic digestion on the resistome profile of dairy manure.","volume":"315","author":"Flores-Orozco","year":"2020","journal-title":"Bioresour. Technol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"2080","DOI":"10.1016\/j.wasman.2014.07.020","article-title":"Investigation into the effect of high concentrations of volatile fatty acids in anaerobic digestion on methanogenic communities.","volume":"34","author":"Franke-Whittle","year":"2014","journal-title":"Waste Manag."},{"key":"B21","doi-asserted-by":"publisher","first-page":"3718","DOI":"10.1093\/bioinformatics\/btv428","article-title":"dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering.","volume":"31","author":"Galili","year":"2015","journal-title":"Bioinformatics"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1186\/s13068-015-0309-9","article-title":"Microbial community dynamics in replicate anaerobic digesters exposed sequentially to increasing organic loading rate, acidosis, and process recovery.","volume":"8","author":"Goux","year":"2015","journal-title":"Biotechnol. Biofuels"},{"key":"B23","doi-asserted-by":"publisher","first-page":"2847","DOI":"10.1093\/bioinformatics\/btw313","article-title":"Complex heatmaps reveal patterns and correlations in multidimensional genomic data.","volume":"32","author":"Gu","year":"2016","journal-title":"Bioinformatics"},{"key":"B24","article-title":"Past: paleontological statistics software package for education and data analysis.","volume":"4","author":"Hammer","year":"2001","journal-title":"Palaeontol. Electron."},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1016\/j.chemosphere.2020.126840","article-title":"Reversibility of propionic acid inhibition to anaerobic digestion: inhibition kinetics and microbial mechanism.","volume":"255","author":"Han","year":"2020","journal-title":"Chemosphere"},{"key":"B26","doi-asserted-by":"publisher","first-page":"330","DOI":"10.1016\/j.syapm.2013.03.006","article-title":"Metagenome and metaproteome analyses of microbial communities in mesophilic biogas-producing anaerobic batch fermentations indicate concerted plant carbohydrate degradation.","volume":"36","author":"Hanreich","year":"2013","journal-title":"Syst. Appl. Microbiol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"1623","DOI":"10.1128\/AEM.72.2.1623-1630.2006","article-title":"Dynamic transition of a methanogenic population in response to the concentration of volatile fatty acids in a thermophilic anaerobic digester.","volume":"72","author":"Hori","year":"2006","journal-title":"Appl. Environ. Microbiol."},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0014519","article-title":"Comparative and joint analysis of two metagenomic datasets from a biogas fermenter obtained by 454-pyrosequencing.","volume":"6","author":"Jaenicke","year":"2011","journal-title":"PLoS One"},{"key":"B29","doi-asserted-by":"publisher","first-page":"1231","DOI":"10.13031\/trans.13462","article-title":"Microbial population change in anaerobic digestion during copper sulfate inhibition and recovery.","volume":"62","author":"Jordaan","year":"2019","journal-title":"Trans. ASABE"},{"key":"B30","doi-asserted-by":"publisher","first-page":"7115","DOI":"10.1128\/AEM.00739-09","article-title":"Rumen microbiome composition determined using two nutritional models of subacute ruminal acidosis.","volume":"75","author":"Khafipour","year":"2009","journal-title":"Appl. Environ. Microbiol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"442","DOI":"10.1101\/gr.7136508","article-title":"The genome of Pelotomaculum thermopropionicum reveals niche-associated evolution in anaerobic microbiota.","volume":"18","author":"Kosaka","year":"2008","journal-title":"Genome Res."},{"key":"B32","doi-asserted-by":"publisher","first-page":"35","DOI":"10.3390\/bioengineering2010035","article-title":"Microbial community shifts during biogas production from biowaste and\/or propionate.","volume":"2","author":"Li","year":"2015","journal-title":"Bioengineering"},{"key":"B33","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1016\/j.biortech.2015.04.015","article-title":"Dynamics of microbial community in a mesophilic anaerobic digester treating food waste: relationship between community structure and process stability.","volume":"189","author":"Li","year":"2015","journal-title":"Bioresour. Technol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"4771","DOI":"10.1007\/s00253-014-5629-3","article-title":"Straw- and slurry-associated prokaryotic communities differ during co-fermentation of straw and swine manure.","volume":"98","author":"Li","year":"2014","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"158","DOI":"10.1016\/j.isci.2018.11.030","article-title":"Graphene facilitates biomethane production from protein-derived Glycine in anaerobic digestion.","volume":"10","author":"Lin","year":"2018","journal-title":"iScience"},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2018.01551","article-title":"Concerted metabolic shifts give new insights into the syntrophic mechanism between propionate-fermenting Pelotomaculum thermopropionicum and hydrogenotrophic Methanocella conradii.","volume":"9","author":"Liu","year":"2018","journal-title":"Front. Microbiol."},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.3390\/ijerph15071399","article-title":"Characterization and dynamic shift of microbial communities during start-up, overloading and steady state in an anaerobic membrane bioreactor.","volume":"15","author":"Martin Vincent","year":"2018","journal-title":"Int. J. Environ. Res. Public Health"},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2105-13-31","article-title":"PANDAseq: paired-end assembler for illumina sequences.","volume":"13","author":"Masella","year":"2012","journal-title":"BMC Bioinform."},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0061217","article-title":"phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data.","volume":"8","author":"McMurdie","year":"2013","journal-title":"PLoS One"},{"key":"B40","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2016.00462","article-title":"Carrageenan gum and adherent invasive Escherichia coli in a piglet model of inflammatory bowel disease: impact on intestinal mucosa-associated microbiota.","volume":"7","author":"Munyaka","year":"2016","journal-title":"Front. Microbiol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"3730","DOI":"10.1016\/j.biortech.2010.11.119","article-title":"A meta-analysis of the microbial diversity observed in anaerobic digesters.","volume":"102","author":"Nelson","year":"2011","journal-title":"Bioresour. Technol."},{"key":"B42","first-page":"631","article-title":"The vegan package.","volume":"10","author":"Oksanen","year":"2007","journal-title":"Commun. Ecol. Pack."},{"key":"B43","doi-asserted-by":"publisher","DOI":"10.3390\/microorganisms6010015","article-title":"Comparison of rumen and manure microbiomes and implications for the inoculation of anaerobic digesters.","volume":"6","author":"Ozbayram","year":"2018","journal-title":"Microorganisms"},{"key":"B44","doi-asserted-by":"publisher","first-page":"296","DOI":"10.1016\/j.watres.2016.05.041","article-title":"Community shifts within anaerobic digestion microbiota facing phenol inhibition: towards early warning microbial indicators.","volume":"100","author":"Poirier","year":"2016","journal-title":"Water Res."},{"key":"B45","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1016\/s0960-8524(00)00187-5","article-title":"Stable performance of anaerobic digestion in the presence of a high concentration of propionic acid.","volume":"78","author":"Pullammanappallil","year":"2001","journal-title":"Bioresour. Technol."},{"key":"B46","doi-asserted-by":"publisher","DOI":"10.7717\/peerj.545","article-title":"Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences.","volume":"2","author":"Rideout","year":"2014","journal-title":"PeerJ"},{"key":"B47","doi-asserted-by":"publisher","first-page":"1081","DOI":"10.1099\/00207713-52-4-1081","article-title":"Methanobrevibacter acididurans sp. nov., a novel methanogen from a sour anaerobic digester.","volume":"52","author":"Savant","year":"2002","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"B48","doi-asserted-by":"publisher","first-page":"5648","DOI":"10.1016\/j.biortech.2009.06.033","article-title":"Population dynamics at digester overload conditions.","volume":"100","author":"Schoen","year":"2009","journal-title":"Bioresour. Technol."},{"key":"B49","doi-asserted-by":"publisher","first-page":"401","DOI":"10.1007\/s00253-005-0275-4","article-title":"Microbial community of a mesophilic propionate-degrading methanogenic consortium in chemostat cultivation analyzed based on 16S rRNA and acetate kinase genes.","volume":"72","author":"Shigematsu","year":"2006","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"B50","doi-asserted-by":"publisher","first-page":"612","DOI":"10.1111\/1574-6941.12148","article-title":"454 pyrosequencing analyses of bacterial and archaeal richness in 21 full-scale biogas digesters.","volume":"85","author":"Sundberg","year":"2013","journal-title":"FEMS Microbiol. Ecol."},{"key":"B51","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1016\/j.wasman.2017.12.005","article-title":"Pre-treatment and inoculum affect the microbial community structure and enhance the biogas reactor performance in a pilot-scale biodigestion of municipal solid waste.","volume":"73","author":"Ventorino","year":"2018","journal-title":"Waste Manag."},{"key":"B52","doi-asserted-by":"publisher","first-page":"5261","DOI":"10.1128\/AEM.00062-07","article-title":"Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy.","volume":"73","author":"Wang","year":"2007","journal-title":"Appl. Environ. Microbiol."},{"key":"B53","author":"Wei","year":"2016","journal-title":"corrplot: Visualization of a Correlation Matrix, R Package Version 0.77."},{"key":"B54","doi-asserted-by":"publisher","first-page":"2702","DOI":"10.1038\/ismej.2016.53","article-title":"RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria.","volume":"10","author":"Wrighton","year":"2016","journal-title":"ISME"},{"key":"B55","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1016\/j.ecoenv.2018.04.016","article-title":"Changes in bacterial community structure and antibiotic resistance genes in soil in the vicinity of a pharmaceutical factory.","volume":"158","author":"Zhu","year":"2018","journal-title":"Ecotoxicol. Environ. Saf."}],"container-title":["Frontiers in Bioengineering and Biotechnology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fbioe.2020.604838\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,12,11]],"date-time":"2020-12-11T08:05:24Z","timestamp":1607673924000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fbioe.2020.604838\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,12,11]]},"references-count":55,"alternative-id":["10.3389\/fbioe.2020.604838"],"URL":"https:\/\/doi.org\/10.3389\/fbioe.2020.604838","relation":{},"ISSN":["2296-4185"],"issn-type":[{"value":"2296-4185","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,12,11]]},"article-number":"604838"}}