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Significant release and microbial utilization of amino sugars and D-amino acid enantiomers from microbial cell wall decomposition in soils

Amino sugars and D-amino acid enantiomers are major components of bacterial and fungal cell walls (i.e. peptidoglycan and chitin) and are often used as biomarkers of microbial residue turnover in soils. However, little is known about the in situ decomposition rates of microbial cell wall residues an...

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Autores principales: Hu, Yuntao, Zheng, Qing, Zhang, Shasha, Noll, Lisa, Wanek, Wolfgang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6774783/
https://www.ncbi.nlm.nih.gov/pubmed/31579317
http://dx.doi.org/10.1016/j.soilbio.2018.04.024
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author Hu, Yuntao
Zheng, Qing
Zhang, Shasha
Noll, Lisa
Wanek, Wolfgang
author_facet Hu, Yuntao
Zheng, Qing
Zhang, Shasha
Noll, Lisa
Wanek, Wolfgang
author_sort Hu, Yuntao
collection PubMed
description Amino sugars and D-amino acid enantiomers are major components of bacterial and fungal cell walls (i.e. peptidoglycan and chitin) and are often used as biomarkers of microbial residue turnover in soils. However, little is known about the in situ decomposition rates of microbial cell wall residues and how soil physicochemical properties affect this process. In this study, we investigated the in situ gross production and consumption rates of free amino sugars (glucosamine and muramic acid) and amino acids (meso-diaminopimelic acid, l-alanine, and d-alanine) by a novel isotope pool dilution assay using (15)N-labeled amino compounds. Soils were obtained from six sites differing in land management (cropland, pasture, and forest) and bedrock (silicate and limestone) and incubated at three temperatures (5, 15, and 25 °C). Free glucosamine released during the decomposition of peptidoglycan and chitin contributed significantly to the extractable soil organic nitrogen pool. Gross production and consumption rates of glucosamine were higher than those of individual amino acids, i.e. L- and D-alanine. Muramic acid had a longer mean residence time (68 h compared to 2.7 h for glucosamine, L- and D-alanine) and made a negligible contribution to soil organic nitrogen fluxes, indicating that free muramic acid was not a major decomposition product of peptidoglycan in soils. Meso-diaminopimelic acid and D-alanine exhibited comparable gross production and consumption rates with L-alanine. These amino acids can be used as indicators to estimate the decomposition of peptidoglycan from bacterial cell wall residues. We found that chitin decomposition was greater in silicate soils, while peptidoglycan decomposition dominated in limestone soils. Glucosamine production rates were not correlated with soil total amino sugars, microbial community structure, or hydrolytic enzyme activities, but were highest in soils with low pH and high sand content, indicating that soil texture and soil pH may strongly influence the decomposition of amino sugar polymers. In contrast, mDAP, L- and D-alanine gross production and consumption rates were positively correlated with soil pH and clay content, due to greater depolymerization of peptidoglycan stem peptides in limestone soils. This isotope pool dilution approach strongly improves our understanding of the mechanisms and environmental controls on microbial cell wall decomposition in soils.
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spelling pubmed-67747832019-10-02 Significant release and microbial utilization of amino sugars and D-amino acid enantiomers from microbial cell wall decomposition in soils Hu, Yuntao Zheng, Qing Zhang, Shasha Noll, Lisa Wanek, Wolfgang Soil Biol Biochem Article Amino sugars and D-amino acid enantiomers are major components of bacterial and fungal cell walls (i.e. peptidoglycan and chitin) and are often used as biomarkers of microbial residue turnover in soils. However, little is known about the in situ decomposition rates of microbial cell wall residues and how soil physicochemical properties affect this process. In this study, we investigated the in situ gross production and consumption rates of free amino sugars (glucosamine and muramic acid) and amino acids (meso-diaminopimelic acid, l-alanine, and d-alanine) by a novel isotope pool dilution assay using (15)N-labeled amino compounds. Soils were obtained from six sites differing in land management (cropland, pasture, and forest) and bedrock (silicate and limestone) and incubated at three temperatures (5, 15, and 25 °C). Free glucosamine released during the decomposition of peptidoglycan and chitin contributed significantly to the extractable soil organic nitrogen pool. Gross production and consumption rates of glucosamine were higher than those of individual amino acids, i.e. L- and D-alanine. Muramic acid had a longer mean residence time (68 h compared to 2.7 h for glucosamine, L- and D-alanine) and made a negligible contribution to soil organic nitrogen fluxes, indicating that free muramic acid was not a major decomposition product of peptidoglycan in soils. Meso-diaminopimelic acid and D-alanine exhibited comparable gross production and consumption rates with L-alanine. These amino acids can be used as indicators to estimate the decomposition of peptidoglycan from bacterial cell wall residues. We found that chitin decomposition was greater in silicate soils, while peptidoglycan decomposition dominated in limestone soils. Glucosamine production rates were not correlated with soil total amino sugars, microbial community structure, or hydrolytic enzyme activities, but were highest in soils with low pH and high sand content, indicating that soil texture and soil pH may strongly influence the decomposition of amino sugar polymers. In contrast, mDAP, L- and D-alanine gross production and consumption rates were positively correlated with soil pH and clay content, due to greater depolymerization of peptidoglycan stem peptides in limestone soils. This isotope pool dilution approach strongly improves our understanding of the mechanisms and environmental controls on microbial cell wall decomposition in soils. 2018-05-16 2018-08 /pmc/articles/PMC6774783/ /pubmed/31579317 http://dx.doi.org/10.1016/j.soilbio.2018.04.024 Text en http://creativecommons.org/licenses/BY-NC-ND/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/).
spellingShingle Article
Hu, Yuntao
Zheng, Qing
Zhang, Shasha
Noll, Lisa
Wanek, Wolfgang
Significant release and microbial utilization of amino sugars and D-amino acid enantiomers from microbial cell wall decomposition in soils
title Significant release and microbial utilization of amino sugars and D-amino acid enantiomers from microbial cell wall decomposition in soils
title_full Significant release and microbial utilization of amino sugars and D-amino acid enantiomers from microbial cell wall decomposition in soils
title_fullStr Significant release and microbial utilization of amino sugars and D-amino acid enantiomers from microbial cell wall decomposition in soils
title_full_unstemmed Significant release and microbial utilization of amino sugars and D-amino acid enantiomers from microbial cell wall decomposition in soils
title_short Significant release and microbial utilization of amino sugars and D-amino acid enantiomers from microbial cell wall decomposition in soils
title_sort significant release and microbial utilization of amino sugars and d-amino acid enantiomers from microbial cell wall decomposition in soils
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6774783/
https://www.ncbi.nlm.nih.gov/pubmed/31579317
http://dx.doi.org/10.1016/j.soilbio.2018.04.024
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