{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,21]],"date-time":"2026-04-21T06:20:31Z","timestamp":1776752431432,"version":"3.51.2"},"update-to":[{"DOI":"10.1371\/journal.pcbi.1010491","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,9,28]],"date-time":"2022-09-28T00:00:00Z","timestamp":1664323200000}}],"reference-count":59,"publisher":"Public Library of Science (PLoS)","issue":"9","license":[{"start":{"date-parts":[[2022,9,9]],"date-time":"2022-09-09T00:00:00Z","timestamp":1662681600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003246","name":"Nederlandse Organisatie voor Wetenschappelijk Onderzoek","doi-asserted-by":"publisher","award":["645.001.002"],"award-info":[{"award-number":["645.001.002"]}],"id":[{"id":"10.13039\/501100003246","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100007192","name":"Rijksinstituut voor Volksgezondheid en Milieu","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100007192","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Unraveling the network of interactions in ecological communities is a daunting task. Common methods to infer interspecific interactions from cross-sectional data are based on co-occurrence measures. For instance, interactions in the human microbiome are often inferred from correlations between the abundances of bacterial phylogenetic groups across subjects. We tested whether such correlation-based methods are indeed reliable for inferring interaction networks. For this purpose, we simulated bacterial communities by means of the generalized Lotka-Volterra model, with variation in model parameters representing variability among hosts. Our results show that correlations can be indicative for presence of bacterial interactions, but only when measurement noise is low relative to the variation in interaction strengths between hosts. Indication of interaction was affected by type of interaction network, process noise and sampling under non-equilibrium conditions. The sign of a correlation mostly coincided with the nature of the strongest pairwise interaction, but this is not necessarily the case. For instance, under rare conditions of identical interaction strength, we found that competitive and exploitative interactions can result in positive as well as negative correlations. Thus, cross-sectional abundance data carry limited information on specific interaction types. Correlations in abundance may hint at interactions but require independent validation.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1010491","type":"journal-article","created":{"date-parts":[[2022,9,9]],"date-time":"2022-09-09T21:05:15Z","timestamp":1662757515000},"page":"e1010491","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":31,"title":["Species abundance correlations carry limited information about microbial network interactions"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7422-9519","authenticated-orcid":true,"given":"Susanne","family":"Pinto","sequence":"first","affiliation":[]},{"given":"Elisa","family":"Beninc\u00e0","sequence":"additional","affiliation":[]},{"given":"Egbert H.","family":"van 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Cho","year":"2012","journal-title":"Nature Reviews Genetics"},{"key":"pcbi.1010491.ref027","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s40168-020-0793-4","article-title":"Separating the signal from the noise in metagenomic cell-free DNA sequencing","volume":"8","author":"P Burnham","year":"2020","journal-title":"Microbiome"},{"key":"pcbi.1010491.ref028","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1063\/1.168540","article-title":"Algorithms and software for ordinary differential equations and differential algebraic equations, Part II: Higher-order methods and software packages","volume":"9","author":"AC Hindmarsh","year":"1995","journal-title":"Computers in Physics"},{"issue":"20","key":"pcbi.1010491.ref029","doi-asserted-by":"crossref","first-page":"12583","DOI":"10.1073\/pnas.202301299","article-title":"Classification of scale-free networks.","volume":"99","author":"OE Goh 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Sasaki","year":"2007","journal-title":"University of Manchester: School of Computer Science"},{"key":"pcbi.1010491.ref034","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0200458","article-title":"Rarity of microbial species: In search of reliable associations.","volume":"14","author":"A Cougoul","year":"2019","journal-title":"PLoS ONE"},{"key":"pcbi.1010491.ref035","first-page":"1","article-title":"Environmental shaping of the bacterial and fungal community in infant bed dust and correlations with the airway microbiota.","volume":"7","author":"S Gupta","year":"2020","journal-title":"Microbiome"},{"key":"pcbi.1010491.ref036","doi-asserted-by":"crossref","first-page":"1063","DOI":"10.1007\/s00248-017-1079-7","article-title":"The P\/N (Positive-to-Negative Links) ratio in complex networks\u2014a promising in silico biomarker for detecting changes occurring in the human microbiome.","volume":"75","author":"ZS Ma","year":"2018","journal-title":"Microbial Ecology"},{"key":"pcbi.1010491.ref037","first-page":"1","article-title":"Antibiotics create a shift from mutualism to competition in human gut communities with a longer-lasting impact on fungi than bacteria","volume":"12","author":"B Seelbinder","year":"2020","journal-title":"Microbiome"},{"key":"pcbi.1010491.ref038","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1093\/femsre\/fuy030","article-title":"From hairballs to hypotheses-biological insights from microbial networks","volume":"42","author":"L R\u00f6ttjers","year":"2018","journal-title":"FEMS Microbiology Reviews"},{"issue":"2","key":"pcbi.1010491.ref039","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1038\/s41559-020-01353-4","article-title":"Polarization of microbial communities between competitive and cooperative metabolism","volume":"5","author":"D Machado","year":"2021","journal-title":"Nat Ecol Evol"},{"key":"pcbi.1010491.ref040","doi-asserted-by":"crossref","first-page":"947","DOI":"10.2307\/1941551","article-title":"Conditions for a species to gain advantage from the presence of competitors","volume":"72","author":"L Stone","year":"1991","journal-title":"Ecology"},{"key":"pcbi.1010491.ref041","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0102451","article-title":"Identifying keystone species in the human gut microbiome from metagenomic timeseries using sparse linear regression","volume":"9","author":"CK Fisher","year":"2014","journal-title":"PLoS ONE"},{"key":"pcbi.1010491.ref042","first-page":"690","article-title":"Species co-occurrence networks: can they reveal trophic and non-trophic interactions in ecological communities?","volume":"99","author":"MA Freilich","year":"2018","journal-title":"The Ecological Society of America"},{"issue":"0062","key":"pcbi.1010491.ref043","article-title":"Higher-order interactions capture unexplained complexity in diverse communities.","volume":"1","author":"M Mayfield","year":"2017","journal-title":"Nat Ecol Evol"},{"key":"pcbi.1010491.ref044","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1086\/284672","article-title":"The importance of the mechanisms of interspecific competition","volume":"129","author":"D. Tilman","year":"1987","journal-title":"The American Naturalist"},{"key":"pcbi.1010491.ref045","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1016\/S0169-5347(99)01723-1","article-title":"Trophic cascades revealed in diverse ecosystems","volume":"14","author":"M Pace","year":"1999","journal-title":"Trends in Ecology and Evolution"},{"key":"pcbi.1010491.ref046","doi-asserted-by":"crossref","first-page":"1","DOI":"10.7554\/eLife.25051","article-title":"Lotka-Volterra pairwise modeling fails to capture diverse pairwise microbial interactions.","volume":"6","author":"B Momeni","year":"2017","journal-title":"eLife"},{"key":"pcbi.1010491.ref047","doi-asserted-by":"crossref","DOI":"10.1007\/978-1-4614-2299-0","volume-title":"Graphical models with R","author":"S H\u00f8jsgaard","year":"2012"},{"issue":"1","key":"pcbi.1010491.ref048","doi-asserted-by":"crossref","first-page":"151","DOI":"10.2307\/1939391","article-title":"Predicting Direct and Indirect Effects: An Integrated Approach Using Experiments and Path Analysis","volume":"75","author":"J. Wootton","year":"1994","journal-title":"Ecology"},{"key":"pcbi.1010491.ref049","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fmicb.2015.00213","article-title":"Systems modeling approaches for microbial community studies: from metagenomics to inference of the community structure","volume":"6","author":"M Hanemaaijer","year":"2015","journal-title":"Frontiers in Microbiology"},{"key":"pcbi.1010491.ref050","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1042\/BST20170265","article-title":"Review and perspective on mathematical modeling of microbial ecosystems","volume":"46","author":"A Succurro","year":"2018","journal-title":"Biochemical Society Transactions"},{"key":"pcbi.1010491.ref051","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/S0169-5347(00)01902-9","article-title":"Lifestyle evolution in symbiotic bacteria: Insights from genomics","volume":"15","author":"NA Moran","year":"2000","journal-title":"Trends in Ecology and Evolution"},{"key":"pcbi.1010491.ref052","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1038\/35098000","article-title":"Catastrophic shifts in ecosystems","volume":"413","author":"M Scheffer","year":"2001","journal-title":"Nature"},{"key":"pcbi.1010491.ref053","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1126\/science.275.5298.389","article-title":"Chaotic dynamics in an insect population","volume":"275","author":"RF Costantino","year":"1997","journal-title":"Science"},{"key":"pcbi.1010491.ref054","doi-asserted-by":"crossref","first-page":"1226","DOI":"10.1038\/nature03627","article-title":"Experimental demonstration of chaos in a microbial food web","volume":"435","author":"L Becks","year":"2005","journal-title":"Nature"},{"key":"pcbi.1010491.ref055","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1038\/nature06512","article-title":"Chaos in a long-term experiment with a plankton community","volume":"451","author":"E Beninc\u00e0","year":"2008","journal-title":"Nature"},{"issue":"20","key":"pcbi.1010491.ref056","doi-asserted-by":"crossref","first-page":"6389","DOI":"10.1073\/pnas.1421968112","article-title":"Species fluctuations sustained by a cyclic succession at the edge of chaos","volume":"112","author":"E Beninc\u00e0","year":"2015","journal-title":"Proceedings of the National Academy of Science"},{"key":"pcbi.1010491.ref057","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/ncomms5344","article-title":"Tipping elements in the human intestinal ecosystem","volume":"5","author":"L Lahti","year":"2014","journal-title":"Nature communications"},{"key":"pcbi.1010491.ref058","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1038\/nature08227","article-title":"Early-warning signals for critical transitions","volume":"461","author":"M Scheffer","year":"2009","journal-title":"Nature"},{"key":"pcbi.1010491.ref059","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1126\/science.1225244","article-title":"Anticipating Critical Transitions.","volume":"338","author":"M Scheffer","year":"2012","journal-title":"Science"}],"updated-by":[{"DOI":"10.1371\/journal.pcbi.1010491","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2022,9,28]],"date-time":"2022-09-28T00:00:00Z","timestamp":1664323200000}}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010491","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,3]],"date-time":"2024-10-03T16:00:53Z","timestamp":1727971253000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010491"}},"subtitle":[],"editor":[{"given":"Kiran Raosaheb","family":"Patil","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2022,9,9]]},"references-count":59,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,9,9]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1010491","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.pcbi.1010491","asserted-by":"object"}]},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9,9]]}}}