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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Main Authors: Olivier Crouzet, Laurent Consentino, Jean-Pierre Pétraud, Christelle Marrauld, Jean-Pierre Aguer, Sylvie Bureau, Carine Le Bourvellec, Line Touloumet, Annette Bérard
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.01319/full
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author Olivier Crouzet
Laurent Consentino
Jean-Pierre Pétraud
Christelle Marrauld
Jean-Pierre Aguer
Sylvie Bureau
Carine Le Bourvellec
Line Touloumet
Annette Bérard
author_facet Olivier Crouzet
Laurent Consentino
Jean-Pierre Pétraud
Christelle Marrauld
Jean-Pierre Aguer
Sylvie Bureau
Carine Le Bourvellec
Line Touloumet
Annette Bérard
author_sort Olivier Crouzet
collection DOAJ
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/SignificanceEdaphic 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 doaj.art-467ec5f89fe7490d8ef7b32c8306771b2022-12-21T19:55:22ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-06-011010.3389/fmicb.2019.01319443684Soil Photosynthetic Microbial Communities Mediate Aggregate Stability: Influence of Cropping Systems and Herbicide Use in an Agricultural SoilOlivier Crouzet0Laurent Consentino1Jean-Pierre Pétraud2Christelle Marrauld3Jean-Pierre Aguer4Sylvie Bureau5Carine Le Bourvellec6Line Touloumet7Annette Bérard8UMR ECOSYS (Ecologie et Ecotoxicologie des Agroécosystèmes), INRA, AgroParisTech, Université Paris-Saclay, Versailles, FranceUMR ECOSYS (Ecologie et Ecotoxicologie des Agroécosystèmes), INRA, AgroParisTech, Université Paris-Saclay, Versailles, FranceUMR ECOSYS (Ecologie et Ecotoxicologie des Agroécosystèmes), INRA, AgroParisTech, Université Paris-Saclay, Versailles, FranceUMR ECOSYS (Ecologie et Ecotoxicologie des Agroécosystèmes), INRA, AgroParisTech, Université Paris-Saclay, Versailles, FranceUMR 6023 LMGE, CNRS, Université Clermont Auvergne, Aubière, FranceUMR 408 SQPOV, INRA, Avignon Université, Avignon, FranceUMR 408 SQPOV, INRA, Avignon Université, Avignon, FranceUMR 408 SQPOV, INRA, Avignon Université, Avignon, FranceUMR 1114 EMMAH (Environnement Méditerranéen et Modélisation des Agro-Hydrosystèmes), INRA, Avignon Université, Avignon, FranceEdaphic 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/SignificanceEdaphic 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.https://www.frontiersin.org/article/10.3389/fmicb.2019.01319/fullphotosynthetic microbial communitiescyanobacteriaaggregate stabilityherbicidecropping systemsexopolysaccharides
spellingShingle Olivier Crouzet
Laurent Consentino
Jean-Pierre Pétraud
Christelle Marrauld
Jean-Pierre Aguer
Sylvie Bureau
Carine Le Bourvellec
Line Touloumet
Annette Bérard
Soil Photosynthetic Microbial Communities Mediate Aggregate Stability: Influence of Cropping Systems and Herbicide Use in an Agricultural Soil
Frontiers in Microbiology
photosynthetic microbial communities
cyanobacteria
aggregate stability
herbicide
cropping systems
exopolysaccharides
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 photosynthetic microbial communities
cyanobacteria
aggregate stability
herbicide
cropping systems
exopolysaccharides
url https://www.frontiersin.org/article/10.3389/fmicb.2019.01319/full
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