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Disentangling environmental effects in microbial association networks

BACKGROUND: Ecological interactions among microorganisms are fundamental for ecosystem function, yet they are mostly unknown or poorly understood. High-throughput-omics can indicate microbial interactions through associations across time and space, which can be represented as association networks. A...

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Autores principales: Deutschmann, Ina Maria, Lima-Mendez, Gipsi, Krabberød, Anders K., Raes, Jeroen, Vallina, Sergio M., Faust, Karoline, Logares, Ramiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8620190/
https://www.ncbi.nlm.nih.gov/pubmed/34823593
http://dx.doi.org/10.1186/s40168-021-01141-7
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author Deutschmann, Ina Maria
Lima-Mendez, Gipsi
Krabberød, Anders K.
Raes, Jeroen
Vallina, Sergio M.
Faust, Karoline
Logares, Ramiro
author_facet Deutschmann, Ina Maria
Lima-Mendez, Gipsi
Krabberød, Anders K.
Raes, Jeroen
Vallina, Sergio M.
Faust, Karoline
Logares, Ramiro
author_sort Deutschmann, Ina Maria
collection PubMed
description BACKGROUND: Ecological interactions among microorganisms are fundamental for ecosystem function, yet they are mostly unknown or poorly understood. High-throughput-omics can indicate microbial interactions through associations across time and space, which can be represented as association networks. Associations could result from either ecological interactions between microorganisms, or from environmental selection, where the association is environmentally driven. Therefore, before downstream analysis and interpretation, we need to distinguish the nature of the association, particularly if it is due to environmental selection or not. RESULTS: We present EnDED (environmentally driven edge detection), an implementation of four approaches as well as their combination to predict which links between microorganisms in an association network are environmentally driven. The four approaches are sign pattern, overlap, interaction information, and data processing inequality. We tested EnDED on networks from simulated data of 50 microorganisms. The networks contained on average 50 nodes and 1087 edges, of which 60 were true interactions but 1026 false associations (i.e., environmentally driven or due to chance). Applying each method individually, we detected a moderate to high number of environmentally driven edges—87% sign pattern and overlap, 67% interaction information, and 44% data processing inequality. Combining these methods in an intersection approach resulted in retaining more interactions, both true and false (32% of environmentally driven associations). After validation with the simulated datasets, we applied EnDED on a marine microbial network inferred from 10 years of monthly observations of microbial-plankton abundance. The intersection combination predicted that 8.3% of the associations were environmentally driven, while individual methods predicted 24.8% (data processing inequality), 25.7% (interaction information), and up to 84.6% (sign pattern as well as overlap). The fraction of environmentally driven edges among negative microbial associations in the real network increased rapidly with the number of environmental factors. CONCLUSIONS: To reach accurate hypotheses about ecological interactions, it is important to determine, quantify, and remove environmentally driven associations in marine microbial association networks. For that, EnDED offers up to four individual methods as well as their combination. However, especially for the intersection combination, we suggest using EnDED with other strategies to reduce the number of false associations and consequently the number of potential interaction hypotheses. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01141-7.
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spelling pubmed-86201902021-11-29 Disentangling environmental effects in microbial association networks Deutschmann, Ina Maria Lima-Mendez, Gipsi Krabberød, Anders K. Raes, Jeroen Vallina, Sergio M. Faust, Karoline Logares, Ramiro Microbiome Methodology BACKGROUND: Ecological interactions among microorganisms are fundamental for ecosystem function, yet they are mostly unknown or poorly understood. High-throughput-omics can indicate microbial interactions through associations across time and space, which can be represented as association networks. Associations could result from either ecological interactions between microorganisms, or from environmental selection, where the association is environmentally driven. Therefore, before downstream analysis and interpretation, we need to distinguish the nature of the association, particularly if it is due to environmental selection or not. RESULTS: We present EnDED (environmentally driven edge detection), an implementation of four approaches as well as their combination to predict which links between microorganisms in an association network are environmentally driven. The four approaches are sign pattern, overlap, interaction information, and data processing inequality. We tested EnDED on networks from simulated data of 50 microorganisms. The networks contained on average 50 nodes and 1087 edges, of which 60 were true interactions but 1026 false associations (i.e., environmentally driven or due to chance). Applying each method individually, we detected a moderate to high number of environmentally driven edges—87% sign pattern and overlap, 67% interaction information, and 44% data processing inequality. Combining these methods in an intersection approach resulted in retaining more interactions, both true and false (32% of environmentally driven associations). After validation with the simulated datasets, we applied EnDED on a marine microbial network inferred from 10 years of monthly observations of microbial-plankton abundance. The intersection combination predicted that 8.3% of the associations were environmentally driven, while individual methods predicted 24.8% (data processing inequality), 25.7% (interaction information), and up to 84.6% (sign pattern as well as overlap). The fraction of environmentally driven edges among negative microbial associations in the real network increased rapidly with the number of environmental factors. CONCLUSIONS: To reach accurate hypotheses about ecological interactions, it is important to determine, quantify, and remove environmentally driven associations in marine microbial association networks. For that, EnDED offers up to four individual methods as well as their combination. However, especially for the intersection combination, we suggest using EnDED with other strategies to reduce the number of false associations and consequently the number of potential interaction hypotheses. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-021-01141-7. BioMed Central 2021-11-26 /pmc/articles/PMC8620190/ /pubmed/34823593 http://dx.doi.org/10.1186/s40168-021-01141-7 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Methodology
Deutschmann, Ina Maria
Lima-Mendez, Gipsi
Krabberød, Anders K.
Raes, Jeroen
Vallina, Sergio M.
Faust, Karoline
Logares, Ramiro
Disentangling environmental effects in microbial association networks
title Disentangling environmental effects in microbial association networks
title_full Disentangling environmental effects in microbial association networks
title_fullStr Disentangling environmental effects in microbial association networks
title_full_unstemmed Disentangling environmental effects in microbial association networks
title_short Disentangling environmental effects in microbial association networks
title_sort disentangling environmental effects in microbial association networks
topic Methodology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8620190/
https://www.ncbi.nlm.nih.gov/pubmed/34823593
http://dx.doi.org/10.1186/s40168-021-01141-7
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