{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,7]],"date-time":"2026-04-07T17:35:46Z","timestamp":1775583346576,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1010807","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2023,1,3]],"date-time":"2023-01-03T00:00:00Z","timestamp":1672704000000}}],"reference-count":55,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2022,12,19]],"date-time":"2022-12-19T00:00:00Z","timestamp":1671408000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100020879","name":"James Watt School of Engineering, University of Glasgow","doi-asserted-by":"publisher","award":["EP\/R513222\/1"],"award-info":[{"award-number":["EP\/R513222\/1"]}],"id":[{"id":"10.13039\/501100020879","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>In microbial communities, the ecological interactions between species of different populations are responsible for the spatial distributions observed in aggregates (granules, biofilms or flocs). To explore the underlying mechanisms that control these processes, we have developed a mathematical modelling framework able to describe, label and quantify defined spatial structures that arise from microbial and environmental interactions in communities. An artificial system of three populations collaborating or competing in an aggregate is simulated using individual-based modelling under different environmental conditions. In this study, neutralism, competition, commensalism and concurrence of commensalism and competition have been considered. We were able to identify interspecific segregation of communities that appears in competitive environments (<jats:italic>columned stratification<\/jats:italic>), and a layered distribution of populations that emerges in commensal (<jats:italic>layered stratification<\/jats:italic>). When different ecological interactions were considered in the same aggregate, the resultant spatial distribution was identified as the one controlled by the most limiting substrate. A theoretical modulus was defined, with which we were able to quantify the effect of environmental conditions and ecological interactions to predict the most probable spatial distribution. The specific microbial patterns observed in our results allowed us to identify the optimal spatial organizations for bacteria to thrive when building a microbial community and how this permitted co-existence of populations at different growth rates. Our model reveals that although ecological relationships between different species dictate the distribution of bacteria, the environment controls the final spatial distribution of the community.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1010807","type":"journal-article","created":{"date-parts":[[2022,12,19]],"date-time":"2022-12-19T18:35:37Z","timestamp":1671474937000},"page":"e1010807","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":8,"title":["Environmental and ecological controls of the spatial distribution of microbial populations in aggregates"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0583-3103","authenticated-orcid":true,"given":"Eloi","family":"Martinez-Rabert","sequence":"first","affiliation":[]},{"given":"Chiel","family":"van Amstel","sequence":"additional","affiliation":[]},{"given":"Cindy","family":"Smith","sequence":"additional","affiliation":[]},{"given":"William T.","family":"Sloan","sequence":"additional","affiliation":[]},{"given":"Rebeca","family":"Gonzalez-Cabaleiro","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2022,12,19]]},"reference":[{"issue":"12","key":"pcbi.1010807.ref001","doi-asserted-by":"crossref","first-page":"6578","DOI":"10.1073\/pnas.95.12.6578","article-title":"Prokaryotes: The unseen majority.","volume":"95","author":"WB Whitman","year":"1998","journal-title":"PNAS"},{"issue":"3","key":"pcbi.1010807.ref002","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1086\/693564","article-title":"Inordinate Fondness Multiplied and Redistributed: the Number of Species on Earth and the New Pie of Life","volume":"92","author":"BB Larsen","year":"2017","journal-title":"The Quarterly Review of Biology"},{"issue":"1","key":"pcbi.1010807.ref003","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/s13062-020-00261-8","article-title":"More support for Earth\u2019s massive microbiome.","volume":"15","author":"JT Lennon","year":"2020","journal-title":"Biol Direct."},{"issue":"5879","key":"pcbi.1010807.ref004","doi-asserted-by":"crossref","first-page":"1034","DOI":"10.1126\/science.1153213","article-title":"The Microbial Engines That Drive Earth\u2019s Biogeochemical Cycles","volume":"320","author":"PG Falkowski","year":"2008","journal-title":"Science"},{"issue":"1","key":"pcbi.1010807.ref005","doi-asserted-by":"crossref","first-page":"141","DOI":"10.2307\/3566099","article-title":"A Revised Scheme for the Classification of Population Interactions","volume":"56","author":"W Arthur","year":"1989","journal-title":"Oikos"},{"issue":"1","key":"pcbi.1010807.ref006","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1086\/418432","article-title":"Our Current Understanding of Mutualism","volume":"69","author":"JL Bronstein","year":"1994","journal-title":"The Quarterly Review of Biology"},{"issue":"3","key":"pcbi.1010807.ref007","doi-asserted-by":"crossref","first-page":"R94","DOI":"10.1016\/j.cub.2015.12.021","article-title":"The nitrogen cycle","volume":"26","author":"LY Stein","year":"2016","journal-title":"Current Biology"},{"issue":"1","key":"pcbi.1010807.ref008","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1038\/scientificamerican0178-86","article-title":"How bacteria stick","volume":"238","author":"JW Costerton","year":"1978","journal-title":"Sci Am"},{"issue":"9","key":"pcbi.1010807.ref009","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1038\/nrmicro.2016.94","article-title":"Biofilms: an emergent form of bacterial life","volume":"14","author":"H-C Flemming","year":"2016","journal-title":"Nature Reviews Microbiology"},{"issue":"3106","key":"pcbi.1010807.ref010","article-title":"Non-surface Attached Bacterial Aggregates: A Ubiquitous Third Lifestyle.","volume":"11","author":"Y-M Cai","year":"2020","journal-title":"Frontiers in Microbiology"},{"key":"pcbi.1010807.ref011","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1146\/annurev.micro.54.1.49","article-title":"Biofilm formation as microbial development","volume":"54","author":"G O\u2019Toole","year":"2000","journal-title":"Annu Rev Microbiol"},{"issue":"7","key":"pcbi.1010807.ref012","doi-asserted-by":"crossref","first-page":"1653","DOI":"10.1016\/S0043-1354(01)00379-7","article-title":"The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge","volume":"36","author":"Y Liu","year":"2002","journal-title":"Water Research"},{"issue":"5659","key":"pcbi.1010807.ref013","doi-asserted-by":"crossref","first-page":"793","DOI":"10.1126\/science.1093411","article-title":"Evolutionary Dynamics of Biological Games.","volume":"303","author":"MA Nowak","year":"2004","journal-title":"Science"},{"issue":"1","key":"pcbi.1010807.ref014","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.tibs.2004.11.006","article-title":"Game-theoretical approaches to studying the evolution of biochemical systems","volume":"30","author":"T Pfeiffer","year":"2005","journal-title":"Trends in Biochemical Sciences"},{"issue":"50","key":"pcbi.1010807.ref015","doi-asserted-by":"crossref","first-page":"15450","DOI":"10.1073\/pnas.1506034112","article-title":"Networks of energetic and metabolic interactions define dynamics in microbial communities","volume":"112","author":"M Embree","year":"2015","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"51","key":"pcbi.1010807.ref016","first-page":"E7156","article-title":"Metabolic dependencies drive species co-occurrence in diverse microbial communities","volume":"112","author":"A Zelezniak","year":"2015","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"pcbi.1010807.ref017","article-title":"Species interactions constrain adaptation and preserve ecological stability in an experimental microbial community","author":"JN Barber","year":"2022","journal-title":"The ISME Journal"},{"key":"pcbi.1010807.ref018","article-title":"Interspecific Bacterial Interactions are Reflected in Multispecies Biofilm Spatial Organization.","volume":"7","author":"W Liu","year":"2016","journal-title":"Frontiers in Microbiology"},{"key":"pcbi.1010807.ref019","doi-asserted-by":"crossref","first-page":"e00230","DOI":"10.7554\/eLife.00230","article-title":"Strong inter-population cooperation leads to partner intermixing in microbial communities.","volume":"2","author":"B Momeni","year":"2013","journal-title":"Elife"},{"issue":"3","key":"pcbi.1010807.ref020","doi-asserted-by":"crossref","first-page":"e1000716","DOI":"10.1371\/journal.pcbi.1000716","article-title":"Emergence of Spatial Structure in Cell Groups and the Evolution of Cooperation.","volume":"6","author":"CD Nadell","year":"2010","journal-title":"PLOS Computational Biology"},{"issue":"supplement_2","key":"pcbi.1010807.ref021","doi-asserted-by":"crossref","first-page":"10839","DOI":"10.1073\/pnas.1100292108","article-title":"Social evolution in multispecies biofilms","volume":"108","author":"S Mitri","year":"2011","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"pcbi.1010807.ref022","doi-asserted-by":"crossref","first-page":"e00960","DOI":"10.7554\/eLife.00960","article-title":"Spatial self-organization favors heterotypic cooperation over cheating.","volume":"2","author":"B Momeni","year":"2013","journal-title":"Elife"},{"issue":"3","key":"pcbi.1010807.ref023","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1038\/s41559-019-1080-2","article-title":"Short-range interactions govern the dynamics and functions of microbial communities.","volume":"4","author":"A Dal Co","year":"2020","journal-title":"Nature Ecology & Evolution."},{"issue":"6593","key":"pcbi.1010807.ref024","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1126\/science.abn5093","article-title":"Bacterial species rarely work together","volume":"376","author":"JD Palmer","year":"2022","journal-title":"Science"},{"issue":"11\u201312","key":"pcbi.1010807.ref025","doi-asserted-by":"crossref","first-page":"177","DOI":"10.2166\/wst.2004.0834","article-title":"Assessment of three-dimensional biofilm models through direct comparison with confocal microscopy imaging","volume":"49","author":"JB Xavier","year":"2004","journal-title":"Water Sci Technol"},{"issue":"18","key":"pcbi.1010807.ref026","doi-asserted-by":"crossref","first-page":"6410","DOI":"10.1021\/es070264m","article-title":"Multi-Scale Individual-Based Model of Microbial and Bioconversion Dynamics in Aerobic Granular Sludge.","volume":"41","author":"JB Xavier","year":"2007","journal-title":"Environmental Science & Technology."},{"issue":"96","key":"pcbi.1010807.ref027","doi-asserted-by":"crossref","first-page":"20140172","DOI":"10.1098\/rsif.2014.0172","article-title":"Chemical warfare and survival strategies in bacterial range expansions","volume":"11","author":"MF Weber","year":"2014","journal-title":"Journal of The Royal Society Interface"},{"issue":"1","key":"pcbi.1010807.ref028","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1038\/ismej.2014.174","article-title":"Adhesion as a weapon in microbial competition","volume":"9","author":"J Schluter","year":"2015","journal-title":"The ISME Journal"},{"issue":"6","key":"pcbi.1010807.ref029","doi-asserted-by":"crossref","first-page":"1471","DOI":"10.1038\/ismej.2015.208","article-title":"Resource limitation drives spatial organization in microbial groups","volume":"10","author":"S Mitri","year":"2016","journal-title":"The ISME Journal"},{"issue":"1","key":"pcbi.1010807.ref030","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1038\/s42003-020-01409-y","article-title":"Spatial organization in microbial range expansion emerges from trophic dependencies and successful lineages","volume":"3","author":"B Borer","year":"2020","journal-title":"Communications Biology"},{"issue":"5","key":"pcbi.1010807.ref031","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1038\/s41396-022-01189-9","article-title":"Rare and localized events stabilize microbial community composition and patterns of spatial self-organization in a fluctuating environment","volume":"16","author":"D Ciccarese","year":"2022","journal-title":"The ISME Journal"},{"issue":"6","key":"pcbi.1010807.ref032","doi-asserted-by":"crossref","first-page":"821","DOI":"10.1093\/femsre\/fuaa034","article-title":"Searching for principles of microbial physiology","volume":"44","author":"FJ Bruggeman","year":"2020","journal-title":"FEMS Microbiology Reviews"},{"issue":"2","key":"pcbi.1010807.ref033","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1007\/BF00228619","article-title":"The influence of substrate transport limitation on porosity and methanogenic activity of anaerobic sludge granules","volume":"39","author":"PA Alphenaar","year":"1993","journal-title":"Applied Microbiology and Biotechnology"},{"issue":"4","key":"pcbi.1010807.ref034","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1046\/j.1472-765x.2002.01099.x","article-title":"Specific layers in aerobically grown microbial granules","volume":"34","author":"J-H Tay","year":"2002","journal-title":"Letters in Applied Microbiology"},{"issue":"50","key":"pcbi.1010807.ref035","doi-asserted-by":"crossref","first-page":"19926","DOI":"10.1073\/pnas.0710150104","article-title":"Genetic drift at expanding frontiers promotes gene segregation","volume":"104","author":"O Hallatschek","year":"2007","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"12","key":"pcbi.1010807.ref036","doi-asserted-by":"crossref","first-page":"4641","DOI":"10.1128\/aem.62.12.4641-4647.1996","article-title":"Structure and function of a nitrifying biofilm as determined by in situ hybridization and the use of microelectrodes","volume":"62","author":"A Schramm","year":"1996","journal-title":"Applied and Environmental Microbiology"},{"key":"pcbi.1010807.ref037","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1016\/j.watres.2016.10.028","article-title":"Effects of the residual ammonium concentration on NOB repression during partial nitritation with granular sludge","volume":"106","author":"V Poot","year":"2016","journal-title":"Water Res"},{"issue":"2","key":"pcbi.1010807.ref038","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1111\/j.1574-6941.2008.00470.x","article-title":"Architecture and spatial organization in a triple-species bacterial biofilm synergistically degrading the phenylurea herbicide linuron","volume":"64","author":"P Breugelmans","year":"2008","journal-title":"FEMS Microbiology Ecology"},{"issue":"3","key":"pcbi.1010807.ref039","doi-asserted-by":"crossref","first-page":"1280","DOI":"10.1128\/AEM.65.3.1280-1288.1999","article-title":"Fluorescence in situ hybridization using 16S rRNA-targeted oligonucleotides reveals localization of methanogens and selected uncultured bacteria in mesophilic and thermophilic sludge granules","volume":"65","author":"Y Sekiguchi","year":"1999","journal-title":"Appl Environ Microbiol"},{"issue":"1","key":"pcbi.1010807.ref040","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1046\/j.1462-2920.2000.00084.x","article-title":"Role of commensal relationships on the spatial structure of a surface-attached microbial consortium","volume":"2","author":"AT Nielsen","year":"2000","journal-title":"Environmental Microbiology"},{"issue":"5","key":"pcbi.1010807.ref041","doi-asserted-by":"crossref","first-page":"2495","DOI":"10.1128\/AEM.68.5.2495-2502.2002","article-title":"Metabolic Commensalism and Competition in a Two-Species Microbial Consortium","volume":"68","author":"BB Christensen","year":"2002","journal-title":"Applied and Environmental Microbiology"},{"issue":"2","key":"pcbi.1010807.ref042","doi-asserted-by":"crossref","first-page":"2191","DOI":"10.3390\/ijms15022191","article-title":"Three-Dimensional Stratification of Bacterial Biofilm Populations in a Moving Bed Biofilm Reactor for Nitritation-Anammox","volume":"15","author":"R Almstrand","year":"2014","journal-title":"International Journal of Molecular Sciences"},{"issue":"4","key":"pcbi.1010807.ref043","doi-asserted-by":"crossref","first-page":"1982","DOI":"10.1128\/AEM.70.4.1982-1989.2004","article-title":"Stratification of Activity and Bacterial Community Structure in Biofilms Grown on Membranes Transferring Oxygen","volume":"70","author":"AC Cole","year":"2004","journal-title":"Applied and Environmental Microbiology"},{"key":"pcbi.1010807.ref044","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1016\/j.copbio.2021.01.017","article-title":"Experimental infrastructure requirements for quantitative research on microbial communities","volume":"67","author":"R Kleerebezem","year":"2021","journal-title":"Current Opinion in Biotechnology"},{"issue":"3","key":"pcbi.1010807.ref045","doi-asserted-by":"crossref","first-page":"1273","DOI":"10.1002\/bit.27650","article-title":"How to measure diffusion coefficients in biofilms: A critical analysis","volume":"118","author":"L van den Berg","year":"2021","journal-title":"Biotechnology and Bioengineering"},{"key":"pcbi.1010807.ref046","doi-asserted-by":"crossref","first-page":"100148","DOI":"10.1016\/j.wroa.2022.100148","article-title":"Diffusion of soluble organic substrates in aerobic granular sludge: Effect of molecular weight","volume":"16","author":"L van den Berg","year":"2022","journal-title":"Water Research X"},{"issue":"1","key":"pcbi.1010807.ref047","doi-asserted-by":"crossref","first-page":"5110","DOI":"10.1038\/s41598-019-41542-1","article-title":"Thickness determines microbial community structure and function in nitrifying biofilms via deterministic assembly.","volume":"9","author":"C Suarez","year":"2019","journal-title":"Scientific Reports."},{"issue":"10","key":"pcbi.1010807.ref048","doi-asserted-by":"crossref","first-page":"2475","DOI":"10.1016\/S0043-1354(01)00476-6","article-title":"Completely autotrophic nitrogen removal over nitrite in one single reactor","volume":"36","author":"AO Sliekers","year":"2002","journal-title":"Water Research"},{"issue":"12","key":"pcbi.1010807.ref049","doi-asserted-by":"crossref","first-page":"3809","DOI":"10.1002\/bit.27522","article-title":"Heterogeneous diffusion in aerobic granular sludge","volume":"117","author":"L van den Berg","year":"2020","journal-title":"Biotechnol Bioeng"},{"issue":"7","key":"pcbi.1010807.ref050","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1038\/nrmicro.2016.62","article-title":"Advancing microbial sciences by individual-based modelling","volume":"14","author":"FL Hellweger","year":"2016","journal-title":"Nature Reviews Microbiology"},{"issue":"4","key":"pcbi.1010807.ref051","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1002\/bit.260320404","article-title":"Extended monod kinetics for substrate, product, and cell inhibition","volume":"32","author":"K Han","year":"1988","journal-title":"Biotechnol Bioeng"},{"issue":"11","key":"pcbi.1010807.ref052","doi-asserted-by":"crossref","first-page":"2897","DOI":"10.1099\/00221287-147-11-2897","article-title":"Individual-based modelling of biofilms","volume":"147","author":"JU Kreft","year":"2001","journal-title":"Microbiology"},{"issue":"7","key":"pcbi.1010807.ref053","first-page":"916","article-title":"Relation between Catalytic Activity and Size of Particle. Industrial &","volume":"31","author":"EW Thiele","year":"1939","journal-title":"Engineering Chemistry"},{"issue":"5","key":"pcbi.1010807.ref054","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1111\/j.1472-765X.2005.01695.x","article-title":"Relationship between size and mass transfer resistance in aerobic granules","volume":"40","author":"YQ Liu","year":"2005","journal-title":"Lett Appl Microbiol"},{"issue":"6","key":"pcbi.1010807.ref055","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1007\/s12257-010-0060-9","article-title":"Evaluation of kinetic parameters and mass transfer of glucose-fed granules under hypoxic conditions","volume":"15","author":"Y Chen","year":"2010","journal-title":"Biotechnology and Bioprocess Engineering"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1010807","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2023,1,3]],"date-time":"2023-01-03T00:00:00Z","timestamp":1672704000000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010807","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,3]],"date-time":"2023-01-03T20:03:12Z","timestamp":1672776192000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010807"}},"subtitle":[],"editor":[{"given":"Roeland M. H.","family":"Merks","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2022,12,19]]},"references-count":55,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2022,12,19]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1010807","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.pcbi.1010807","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,12,19]]}}}