How, When, and Where Relic DNA Affects Microbial Diversity

ABSTRACT Extracellular or “relic” DNA is one of the largest pools of nucleic acids in the biosphere. Relic DNA can influence a number of important ecological and evolutionary processes, but it may also affect estimates of microbial abundance and diversity, which has implications for understanding en...

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Autores principales:	J. T. Lennon, M. E. Muscarella, S. A. Placella, B. K. Lehmkuhl
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	biodiversity ecology extracellular DNA mathematical modeling phylogenetic analysis sampling theory Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/003d8e2e84cf4a9090bc06441a43022b
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spelling	oai:doaj.org-article:003d8e2e84cf4a9090bc06441a43022b2021-11-15T16:00:26ZHow, When, and Where Relic DNA Affects Microbial Diversity10.1128/mBio.00637-182150-7511https://doaj.org/article/003d8e2e84cf4a9090bc06441a43022b2018-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00637-18https://doaj.org/toc/2150-7511ABSTRACT Extracellular or “relic” DNA is one of the largest pools of nucleic acids in the biosphere. Relic DNA can influence a number of important ecological and evolutionary processes, but it may also affect estimates of microbial abundance and diversity, which has implications for understanding environmental, engineered, and host-associated ecosystems. We developed models capturing the fundamental processes that regulate the size and composition of the relic DNA pools to identify scenarios leading to biased estimates of biodiversity. Our models predict that bias increases with relic DNA pool size, but only when the species abundance distributions (SADs) of relic and intact DNA are distinct from one another. We evaluated our model predictions by quantifying relic DNA and assessing its contribution to bacterial diversity using 16S rRNA gene sequences collected from different ecosystem types, including soil, sediment, water, and the mammalian gut. On average, relic DNA made up 33% of the total bacterial DNA pool but exceeded 80% in some samples. Despite its abundance, relic DNA had a minimal effect on estimates of taxonomic and phylogenetic diversity, even in ecosystems where processes such as the physical protection of relic DNA are common and predicted by our models to generate bias. Our findings are consistent with the expectation that relic DNA from different taxa degrades at a constant and equal rate, suggesting that it may not fundamentally alter estimates of microbial diversity. IMPORTANCE The ability to rapidly obtain millions of gene sequences and transcripts from a range of environments has greatly advanced understanding of the processes that regulate microbial communities. However, nucleic acids extracted from complex samples do not come only from viable microorganisms. Dead microorganisms can generate large pools of relic DNA that distort insight into the ecology and evolution of microbial systems. Here, we develop a conceptual and quantitative framework for understanding how relic DNA influences the structure of microbiomes. Our theoretical models and empirical results demonstrate that a large relic DNA pool does not automatically lead to biased estimates of microbial diversity. Rather, relic DNA effects emerge in combination with microscale processes that alter the commonness and rarity of sequences found in heterogeneous DNA pools.J. T. LennonM. E. MuscarellaS. A. PlacellaB. K. LehmkuhlAmerican Society for Microbiologyarticlebiodiversityecologyextracellular DNAmathematical modelingphylogenetic analysissampling theoryMicrobiologyQR1-502ENmBio, Vol 9, Iss 3 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	biodiversity ecology extracellular DNA mathematical modeling phylogenetic analysis sampling theory Microbiology QR1-502
spellingShingle	biodiversity ecology extracellular DNA mathematical modeling phylogenetic analysis sampling theory Microbiology QR1-502 J. T. Lennon M. E. Muscarella S. A. Placella B. K. Lehmkuhl How, When, and Where Relic DNA Affects Microbial Diversity
description	ABSTRACT Extracellular or “relic” DNA is one of the largest pools of nucleic acids in the biosphere. Relic DNA can influence a number of important ecological and evolutionary processes, but it may also affect estimates of microbial abundance and diversity, which has implications for understanding environmental, engineered, and host-associated ecosystems. We developed models capturing the fundamental processes that regulate the size and composition of the relic DNA pools to identify scenarios leading to biased estimates of biodiversity. Our models predict that bias increases with relic DNA pool size, but only when the species abundance distributions (SADs) of relic and intact DNA are distinct from one another. We evaluated our model predictions by quantifying relic DNA and assessing its contribution to bacterial diversity using 16S rRNA gene sequences collected from different ecosystem types, including soil, sediment, water, and the mammalian gut. On average, relic DNA made up 33% of the total bacterial DNA pool but exceeded 80% in some samples. Despite its abundance, relic DNA had a minimal effect on estimates of taxonomic and phylogenetic diversity, even in ecosystems where processes such as the physical protection of relic DNA are common and predicted by our models to generate bias. Our findings are consistent with the expectation that relic DNA from different taxa degrades at a constant and equal rate, suggesting that it may not fundamentally alter estimates of microbial diversity. IMPORTANCE The ability to rapidly obtain millions of gene sequences and transcripts from a range of environments has greatly advanced understanding of the processes that regulate microbial communities. However, nucleic acids extracted from complex samples do not come only from viable microorganisms. Dead microorganisms can generate large pools of relic DNA that distort insight into the ecology and evolution of microbial systems. Here, we develop a conceptual and quantitative framework for understanding how relic DNA influences the structure of microbiomes. Our theoretical models and empirical results demonstrate that a large relic DNA pool does not automatically lead to biased estimates of microbial diversity. Rather, relic DNA effects emerge in combination with microscale processes that alter the commonness and rarity of sequences found in heterogeneous DNA pools.
format	article
author	J. T. Lennon M. E. Muscarella S. A. Placella B. K. Lehmkuhl
author_facet	J. T. Lennon M. E. Muscarella S. A. Placella B. K. Lehmkuhl
author_sort	J. T. Lennon
title	How, When, and Where Relic DNA Affects Microbial Diversity
title_short	How, When, and Where Relic DNA Affects Microbial Diversity
title_full	How, When, and Where Relic DNA Affects Microbial Diversity
title_fullStr	How, When, and Where Relic DNA Affects Microbial Diversity
title_full_unstemmed	How, When, and Where Relic DNA Affects Microbial Diversity
title_sort	how, when, and where relic dna affects microbial diversity
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/003d8e2e84cf4a9090bc06441a43022b
work_keys_str_mv	AT jtlennon howwhenandwhererelicdnaaffectsmicrobialdiversity AT memuscarella howwhenandwhererelicdnaaffectsmicrobialdiversity AT saplacella howwhenandwhererelicdnaaffectsmicrobialdiversity AT bklehmkuhl howwhenandwhererelicdnaaffectsmicrobialdiversity
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How, When, and Where Relic DNA Affects Microbial Diversity

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