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Shared Microbial Taxa Respond Predictably to Cyclic Time-Varying Oxygen Limitation in Two Disparate Soils

Periodic oxygen (O(2)) limitation in humid terrestrial soils likely influences microbial composition, but whether communities share similar responses in disparate environments remains unclear. To test if specific microbial taxa share consistent responses to anoxia in radically different soils, we in...

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Autores principales: Hall, Steven J., Huang, Wenjuan, Napieralski, Stephanie A., Roden, Eric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9203030/
https://www.ncbi.nlm.nih.gov/pubmed/35722278
http://dx.doi.org/10.3389/fmicb.2022.866828
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author Hall, Steven J.
Huang, Wenjuan
Napieralski, Stephanie A.
Roden, Eric
author_facet Hall, Steven J.
Huang, Wenjuan
Napieralski, Stephanie A.
Roden, Eric
author_sort Hall, Steven J.
collection PubMed
description Periodic oxygen (O(2)) limitation in humid terrestrial soils likely influences microbial composition, but whether communities share similar responses in disparate environments remains unclear. To test if specific microbial taxa share consistent responses to anoxia in radically different soils, we incubated a rainforest Oxisol and cropland Mollisol under cyclic, time-varying anoxic/oxic cycles in the laboratory. Both soils are known to experience anoxic periods of days to weeks under field conditions; our incubation treatments consisted of anoxic periods of 0, 2, 4, 8, or 12 d followed by 4 d of oxic conditions, repeated for a total of 384 d. Taxa measured by 16S rRNA gene sequences after 48 d and 384 d of experimental treatments varied strongly with increasing anoxic period duration, and responses to anoxia often differed between soils at multiple taxonomic levels. Only 19% of the 30,356 operational taxonomic units (OTUs) occurred in both soils, and most OTUs did not respond consistently to O(2) treatments. However, the OTUs present in both soils were disproportionally abundant, comprising 50% of sequences, and they often had a similar response to anoxic period duration in both soils (p < 0.0001). Overall, 67 OTUs, 36 families, 15 orders, 10 classes, and two phyla had significant and directionally consistent (positive or negative) responses to anoxic period duration in both soils. Prominent OTUs and taxonomic groups increasing with anoxic period duration in both soils included actinomycetes (Micromonosporaceae), numerous Ruminococcaceae, possible metal reducers (Anaeromyxobacter) or oxidizers (Candidatus Koribacter), methanogens (Methanomicrobia), and methanotrophs (Methylocystaceae). OTUs decreasing with anoxic duration in both soils included nitrifiers (Nitrospira) and ubiquitous unidentified Bradyrhizobiaceae and Micromonosporaceae. Even within the same genus, different OTUs occasionally showed strong positive or negative responses to anoxic duration (e.g., Dactylosporangium in the Actinobacteria), highlighting a potential for adaptation or niche partitioning in variable-O(2) environments. Overall, brief anoxic periods impacted the abundance of certain microbial taxa in predictable ways, suggesting that microbial community data may partially reflect and integrate spatiotemporal differences in O(2) availability within and among soils.
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spelling pubmed-92030302022-06-17 Shared Microbial Taxa Respond Predictably to Cyclic Time-Varying Oxygen Limitation in Two Disparate Soils Hall, Steven J. Huang, Wenjuan Napieralski, Stephanie A. Roden, Eric Front Microbiol Microbiology Periodic oxygen (O(2)) limitation in humid terrestrial soils likely influences microbial composition, but whether communities share similar responses in disparate environments remains unclear. To test if specific microbial taxa share consistent responses to anoxia in radically different soils, we incubated a rainforest Oxisol and cropland Mollisol under cyclic, time-varying anoxic/oxic cycles in the laboratory. Both soils are known to experience anoxic periods of days to weeks under field conditions; our incubation treatments consisted of anoxic periods of 0, 2, 4, 8, or 12 d followed by 4 d of oxic conditions, repeated for a total of 384 d. Taxa measured by 16S rRNA gene sequences after 48 d and 384 d of experimental treatments varied strongly with increasing anoxic period duration, and responses to anoxia often differed between soils at multiple taxonomic levels. Only 19% of the 30,356 operational taxonomic units (OTUs) occurred in both soils, and most OTUs did not respond consistently to O(2) treatments. However, the OTUs present in both soils were disproportionally abundant, comprising 50% of sequences, and they often had a similar response to anoxic period duration in both soils (p < 0.0001). Overall, 67 OTUs, 36 families, 15 orders, 10 classes, and two phyla had significant and directionally consistent (positive or negative) responses to anoxic period duration in both soils. Prominent OTUs and taxonomic groups increasing with anoxic period duration in both soils included actinomycetes (Micromonosporaceae), numerous Ruminococcaceae, possible metal reducers (Anaeromyxobacter) or oxidizers (Candidatus Koribacter), methanogens (Methanomicrobia), and methanotrophs (Methylocystaceae). OTUs decreasing with anoxic duration in both soils included nitrifiers (Nitrospira) and ubiquitous unidentified Bradyrhizobiaceae and Micromonosporaceae. Even within the same genus, different OTUs occasionally showed strong positive or negative responses to anoxic duration (e.g., Dactylosporangium in the Actinobacteria), highlighting a potential for adaptation or niche partitioning in variable-O(2) environments. Overall, brief anoxic periods impacted the abundance of certain microbial taxa in predictable ways, suggesting that microbial community data may partially reflect and integrate spatiotemporal differences in O(2) availability within and among soils. Frontiers Media S.A. 2022-06-02 /pmc/articles/PMC9203030/ /pubmed/35722278 http://dx.doi.org/10.3389/fmicb.2022.866828 Text en Copyright © 2022 Hall, Huang, Napieralski and Roden. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Hall, Steven J.
Huang, Wenjuan
Napieralski, Stephanie A.
Roden, Eric
Shared Microbial Taxa Respond Predictably to Cyclic Time-Varying Oxygen Limitation in Two Disparate Soils
title Shared Microbial Taxa Respond Predictably to Cyclic Time-Varying Oxygen Limitation in Two Disparate Soils
title_full Shared Microbial Taxa Respond Predictably to Cyclic Time-Varying Oxygen Limitation in Two Disparate Soils
title_fullStr Shared Microbial Taxa Respond Predictably to Cyclic Time-Varying Oxygen Limitation in Two Disparate Soils
title_full_unstemmed Shared Microbial Taxa Respond Predictably to Cyclic Time-Varying Oxygen Limitation in Two Disparate Soils
title_short Shared Microbial Taxa Respond Predictably to Cyclic Time-Varying Oxygen Limitation in Two Disparate Soils
title_sort shared microbial taxa respond predictably to cyclic time-varying oxygen limitation in two disparate soils
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9203030/
https://www.ncbi.nlm.nih.gov/pubmed/35722278
http://dx.doi.org/10.3389/fmicb.2022.866828
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