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Soil Photosynthetic Microbial Communities Mediate Aggregate Stability: Influence of Cropping Systems and Herbicide Use in an Agricultural Soil

Edaphic cyanobacteria and algae have been extensively studied in dryland soils because they play key roles in the formation of biological soil crusts and the stabilization of soil surfaces. Yet, in temperate agricultural crop soils, little is understood about the functional significance of indigenou...

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Autores principales: Crouzet, Olivier, Consentino, Laurent, Pétraud, Jean-Pierre, Marrauld, Christelle, Aguer, Jean-Pierre, Bureau, Sylvie, Le Bourvellec, Carine, Touloumet, Line, Bérard, Annette
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6587365/
https://www.ncbi.nlm.nih.gov/pubmed/31258520
http://dx.doi.org/10.3389/fmicb.2019.01319
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author Crouzet, Olivier
Consentino, Laurent
Pétraud, Jean-Pierre
Marrauld, Christelle
Aguer, Jean-Pierre
Bureau, Sylvie
Le Bourvellec, Carine
Touloumet, Line
Bérard, Annette
author_facet Crouzet, Olivier
Consentino, Laurent
Pétraud, Jean-Pierre
Marrauld, Christelle
Aguer, Jean-Pierre
Bureau, Sylvie
Le Bourvellec, Carine
Touloumet, Line
Bérard, Annette
author_sort Crouzet, Olivier
collection PubMed
description Edaphic cyanobacteria and algae have been extensively studied in dryland soils because they play key roles in the formation of biological soil crusts and the stabilization of soil surfaces. Yet, in temperate agricultural crop soils, little is understood about the functional significance of indigenous photosynthetic microbial communities for various soil processes. This study investigated how indigenous soil algae and cyanobacteria affected topsoil aggregate stability in cereal cropping systems. Topsoil aggregates from conventional and organic cropping systems were incubated in microcosms under dark or photoperiodic conditions with or without a treatment with an herbicide (isoproturon). Physicochemical parameters (bound exopolysaccharides, organic carbon) and microbial parameters (esterase activity, chlorophyll a biomass, and pigment profiles) were measured for incubated aggregates. Aggregate stability were analyzed on the basis of aggregate size distribution and the mean weight diameter (MWD) index, resulting from disaggregation tests. Soil photosynthetic microbial biomass (chl a) was strongly and positively correlated with aggregate stability indicators. The development of microalgae crusts in photoperiodic conditions induced a strong increase of the largest aggregates (>2 mm), as compared to dark conditions (up to 10.6 fold and 27.1 fold, in soil from organic and conventional cropping systems, respectively). Concomitantly, the MWD significantly increased by 2.4 fold and 4.2 fold, for soil from organic and conventional cropping systems. Soil microalgae may have operated directly via biochemical mechanisms, by producing exopolymeric matrices surrounding soil aggregates (bound exopolysaccharides: 0.39–0.45 μg C g(−1) soil), and via biophysical mechanisms, where filamentous living microbiota enmeshed soil aggregates. In addition, they may have acted indirectly by stimulating heterotrophic microbial communities, as revealed by the positive effect of microalgal growth on total microbial activity. The herbicide treatment negatively impacted soil microalgal community, resulting in significant decreases of the MWD of the conventional soil aggregates (up to −42% of the value in light treatment). This study underscores that indigenous edaphic algae and cyanobacteria can promote aggregate formation, by forming photosynthetic microbiotic crusts, thus improving the structural stability of topsoil, in temperate croplands. However, the herbicide uses can impair the functional abilities of algal and cyanobacterial communities in agricultural soils. ORIGINALITY/SIGNIFICANCE: Edaphic algal and cyanobacterial communities are known to form photosynthetic microbial crusts in arid soils, where they drive key ecosystem functions. Although less well characterized, such communities are also transiently abundant in temperate and mesic cropped soils. This microcosm study investigated the communities’ functional significance in topsoil aggregate formation and stabilization in two temperate cropping systems. Overall, our results showed that the development of indigenous microalgal communities under our experimental conditions drove higher structural stability in topsoil aggregates in temperate cropland soils. Also, herbicide use affected photosynthetic microbial communities and consequently impaired soil aggregation.
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spelling pubmed-65873652019-06-28 Soil Photosynthetic Microbial Communities Mediate Aggregate Stability: Influence of Cropping Systems and Herbicide Use in an Agricultural Soil Crouzet, Olivier Consentino, Laurent Pétraud, Jean-Pierre Marrauld, Christelle Aguer, Jean-Pierre Bureau, Sylvie Le Bourvellec, Carine Touloumet, Line Bérard, Annette Front Microbiol Microbiology Edaphic cyanobacteria and algae have been extensively studied in dryland soils because they play key roles in the formation of biological soil crusts and the stabilization of soil surfaces. Yet, in temperate agricultural crop soils, little is understood about the functional significance of indigenous photosynthetic microbial communities for various soil processes. This study investigated how indigenous soil algae and cyanobacteria affected topsoil aggregate stability in cereal cropping systems. Topsoil aggregates from conventional and organic cropping systems were incubated in microcosms under dark or photoperiodic conditions with or without a treatment with an herbicide (isoproturon). Physicochemical parameters (bound exopolysaccharides, organic carbon) and microbial parameters (esterase activity, chlorophyll a biomass, and pigment profiles) were measured for incubated aggregates. Aggregate stability were analyzed on the basis of aggregate size distribution and the mean weight diameter (MWD) index, resulting from disaggregation tests. Soil photosynthetic microbial biomass (chl a) was strongly and positively correlated with aggregate stability indicators. The development of microalgae crusts in photoperiodic conditions induced a strong increase of the largest aggregates (>2 mm), as compared to dark conditions (up to 10.6 fold and 27.1 fold, in soil from organic and conventional cropping systems, respectively). Concomitantly, the MWD significantly increased by 2.4 fold and 4.2 fold, for soil from organic and conventional cropping systems. Soil microalgae may have operated directly via biochemical mechanisms, by producing exopolymeric matrices surrounding soil aggregates (bound exopolysaccharides: 0.39–0.45 μg C g(−1) soil), and via biophysical mechanisms, where filamentous living microbiota enmeshed soil aggregates. In addition, they may have acted indirectly by stimulating heterotrophic microbial communities, as revealed by the positive effect of microalgal growth on total microbial activity. The herbicide treatment negatively impacted soil microalgal community, resulting in significant decreases of the MWD of the conventional soil aggregates (up to −42% of the value in light treatment). This study underscores that indigenous edaphic algae and cyanobacteria can promote aggregate formation, by forming photosynthetic microbiotic crusts, thus improving the structural stability of topsoil, in temperate croplands. However, the herbicide uses can impair the functional abilities of algal and cyanobacterial communities in agricultural soils. ORIGINALITY/SIGNIFICANCE: Edaphic algal and cyanobacterial communities are known to form photosynthetic microbial crusts in arid soils, where they drive key ecosystem functions. Although less well characterized, such communities are also transiently abundant in temperate and mesic cropped soils. This microcosm study investigated the communities’ functional significance in topsoil aggregate formation and stabilization in two temperate cropping systems. Overall, our results showed that the development of indigenous microalgal communities under our experimental conditions drove higher structural stability in topsoil aggregates in temperate cropland soils. Also, herbicide use affected photosynthetic microbial communities and consequently impaired soil aggregation. Frontiers Media S.A. 2019-06-14 /pmc/articles/PMC6587365/ /pubmed/31258520 http://dx.doi.org/10.3389/fmicb.2019.01319 Text en Copyright © 2019 Crouzet, Consentino, Pétraud, Marrauld, Aguer, Bureau, Le Bourvellec, Touloumet and Bérard. http://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
Crouzet, Olivier
Consentino, Laurent
Pétraud, Jean-Pierre
Marrauld, Christelle
Aguer, Jean-Pierre
Bureau, Sylvie
Le Bourvellec, Carine
Touloumet, Line
Bérard, Annette
Soil Photosynthetic Microbial Communities Mediate Aggregate Stability: Influence of Cropping Systems and Herbicide Use in an Agricultural Soil
title Soil Photosynthetic Microbial Communities Mediate Aggregate Stability: Influence of Cropping Systems and Herbicide Use in an Agricultural Soil
title_full Soil Photosynthetic Microbial Communities Mediate Aggregate Stability: Influence of Cropping Systems and Herbicide Use in an Agricultural Soil
title_fullStr Soil Photosynthetic Microbial Communities Mediate Aggregate Stability: Influence of Cropping Systems and Herbicide Use in an Agricultural Soil
title_full_unstemmed Soil Photosynthetic Microbial Communities Mediate Aggregate Stability: Influence of Cropping Systems and Herbicide Use in an Agricultural Soil
title_short Soil Photosynthetic Microbial Communities Mediate Aggregate Stability: Influence of Cropping Systems and Herbicide Use in an Agricultural Soil
title_sort soil photosynthetic microbial communities mediate aggregate stability: influence of cropping systems and herbicide use in an agricultural soil
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6587365/
https://www.ncbi.nlm.nih.gov/pubmed/31258520
http://dx.doi.org/10.3389/fmicb.2019.01319
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