Prokaryotic Community Composition and Extracellular Polymeric Substances Affect Soil Microaggregation in Carbonate Containing Semiarid Grasslands

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Autoren

  • Jeroen H.T. Zethof
  • Antje Bettermann
  • Cordula Vogel
  • Doreen Babin
  • Erik L.H. Cammeraat
  • Albert Solé-Benet
  • Roberto Lázaro
  • Lourdes Luna
  • Joseph Nesme
  • Susanne K. Woche
  • Søren J. Sørensen
  • Kornelia Smalla
  • Karsten Kalbitz

Externe Organisationen

  • Technische Universität Dresden
  • Julius Kühn-Institut (JKI) Bundesforschungsinstitut für Kulturpflanzen
  • Spanish National Research Council (CSIC)
  • University of Copenhagen
  • Universiteit van Amsterdam (UvA)
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Details

OriginalspracheEnglisch
Aufsatznummer51
FachzeitschriftFrontiers in Environmental Science
Jahrgang8
PublikationsstatusVeröffentlicht - 11 Juni 2020

Abstract

In the barren semiarid landscape individual plant species improve soil structure, reducing the erosion risks, whereby microaggregates form the most fundamental soil structural components. Extracellular polymeric substances (EPS) are considered an important glue determining aggregation in addition to inorganic binding agents such as carbonates. However, the role of the prokaryotic community in EPS formation and consequently for microaggregation in natural environments is not substantially clarified yet. EPS should be particularly important under semiarid conditions as it forms a protection mechanism of the prokaryotes against desiccation. Therefore, we examined the influence of the prokaryotic community on soil EPS content and subsequently on soil microaggregation in semiarid grasslands, depending on the parent material, common plant species and the distance to the plant. Soil samples were taken over a distance gradient from two major semiarid grassland plant species in Southern Spain, the legume shrub Anthyllis cytisoides and the grass tussock Macrochloa tenacissima, to the surrounding bare soil at two sites, rich and poor in carbonates. Total community DNA and EPS were extracted, followed by quantification of EPS-saccharide, bacterial abundance and examination of the prokaryotic community composition. Further, the particle size distribution of the microaggregate fraction was determined as an indication of microaggregation. We found that the overall prokaryotic community composition differed between the two sites, but not between plant species. Nonetheless, a link between the community composition and EPS content was established, whereby soil organic matter (OM) seems to be a regulating factor as increasing soil OM contents resulted in more EPS-saccharide. Furthermore, microaggregation was enhanced by the canopy, especially at the edge of Macrochloa tussocks. Contrary to the expectation that increasing inorganic C contents would diminish importance of EPS, the parent material richest in inorganic C resulted in a significant effect of EPS-saccharide contents on microaggregation according to the structural equation model. For the inorganic C poor site, EPS-saccharide had no observed direct effect on microaggregation. Based on our results we conclude that the availability of decomposable OM influences the prokaryotic community composition and thereby triggers EPS production whereas large contents of polyvalent cations promote the stabilizing effect of EPS on microaggregates.

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Prokaryotic Community Composition and Extracellular Polymeric Substances Affect Soil Microaggregation in Carbonate Containing Semiarid Grasslands. / Zethof, Jeroen H.T.; Bettermann, Antje; Vogel, Cordula et al.
in: Frontiers in Environmental Science, Jahrgang 8, 51, 11.06.2020.

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Zethof, JHT, Bettermann, A, Vogel, C, Babin, D, Cammeraat, ELH, Solé-Benet, A, Lázaro, R, Luna, L, Nesme, J, Woche, SK, Sørensen, SJ, Smalla, K & Kalbitz, K 2020, 'Prokaryotic Community Composition and Extracellular Polymeric Substances Affect Soil Microaggregation in Carbonate Containing Semiarid Grasslands', Frontiers in Environmental Science, Jg. 8, 51. https://doi.org/10.3389/fenvs.2020.00051
Zethof, J. H. T., Bettermann, A., Vogel, C., Babin, D., Cammeraat, E. L. H., Solé-Benet, A., Lázaro, R., Luna, L., Nesme, J., Woche, S. K., Sørensen, S. J., Smalla, K., & Kalbitz, K. (2020). Prokaryotic Community Composition and Extracellular Polymeric Substances Affect Soil Microaggregation in Carbonate Containing Semiarid Grasslands. Frontiers in Environmental Science, 8, Artikel 51. https://doi.org/10.3389/fenvs.2020.00051
Zethof JHT, Bettermann A, Vogel C, Babin D, Cammeraat ELH, Solé-Benet A et al. Prokaryotic Community Composition and Extracellular Polymeric Substances Affect Soil Microaggregation in Carbonate Containing Semiarid Grasslands. Frontiers in Environmental Science. 2020 Jun 11;8:51. doi: 10.3389/fenvs.2020.00051
Zethof, Jeroen H.T. ; Bettermann, Antje ; Vogel, Cordula et al. / Prokaryotic Community Composition and Extracellular Polymeric Substances Affect Soil Microaggregation in Carbonate Containing Semiarid Grasslands. in: Frontiers in Environmental Science. 2020 ; Jahrgang 8.
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@article{7d116023d77943b39297b9a4db8a7beb,
title = "Prokaryotic Community Composition and Extracellular Polymeric Substances Affect Soil Microaggregation in Carbonate Containing Semiarid Grasslands",
abstract = "In the barren semiarid landscape individual plant species improve soil structure, reducing the erosion risks, whereby microaggregates form the most fundamental soil structural components. Extracellular polymeric substances (EPS) are considered an important glue determining aggregation in addition to inorganic binding agents such as carbonates. However, the role of the prokaryotic community in EPS formation and consequently for microaggregation in natural environments is not substantially clarified yet. EPS should be particularly important under semiarid conditions as it forms a protection mechanism of the prokaryotes against desiccation. Therefore, we examined the influence of the prokaryotic community on soil EPS content and subsequently on soil microaggregation in semiarid grasslands, depending on the parent material, common plant species and the distance to the plant. Soil samples were taken over a distance gradient from two major semiarid grassland plant species in Southern Spain, the legume shrub Anthyllis cytisoides and the grass tussock Macrochloa tenacissima, to the surrounding bare soil at two sites, rich and poor in carbonates. Total community DNA and EPS were extracted, followed by quantification of EPS-saccharide, bacterial abundance and examination of the prokaryotic community composition. Further, the particle size distribution of the microaggregate fraction was determined as an indication of microaggregation. We found that the overall prokaryotic community composition differed between the two sites, but not between plant species. Nonetheless, a link between the community composition and EPS content was established, whereby soil organic matter (OM) seems to be a regulating factor as increasing soil OM contents resulted in more EPS-saccharide. Furthermore, microaggregation was enhanced by the canopy, especially at the edge of Macrochloa tussocks. Contrary to the expectation that increasing inorganic C contents would diminish importance of EPS, the parent material richest in inorganic C resulted in a significant effect of EPS-saccharide contents on microaggregation according to the structural equation model. For the inorganic C poor site, EPS-saccharide had no observed direct effect on microaggregation. Based on our results we conclude that the availability of decomposable OM influences the prokaryotic community composition and thereby triggers EPS production whereas large contents of polyvalent cations promote the stabilizing effect of EPS on microaggregates.",
keywords = "16S rRNA gene, Anthyllis cytisoides, EPS, Illumina amplicon sequencing, Macrochloa tenacissima, slightly alkaline soils",
author = "Zethof, {Jeroen H.T.} and Antje Bettermann and Cordula Vogel and Doreen Babin and Cammeraat, {Erik L.H.} and Albert Sol{\'e}-Benet and Roberto L{\'a}zaro and Lourdes Luna and Joseph Nesme and Woche, {Susanne K.} and S{\o}rensen, {S{\o}ren J.} and Kornelia Smalla and Karsten Kalbitz",
note = "Funding information: We thank Stephan Kr{\"u}ger for his mental support and assistance during the sampling campaign, Manuela Unger and Gisela Ciesielski for the laboratory assistance, Tim Schacherl for establishing the microaggregation method and Ilse-Marie Jungkurth for checking the language of the manuscript. Further, we want to thank the Max Planck Institute for Biogeochemistry (Department Biogeochemical Processes, Jena) for the graphitic C measurements. Funding. This study was financially supported by the Deutsche Forschungsgemeinschaft (DFG), Bonn, Germany, under grants KA1737/13-1 and SM 59/18-1 “Extracellular polymeric substances and aggregate stability – how microorganisms affect soil erosion by water.” AS-B, RL, and LL were supported thanks to the Research Project “Biocrust Dynamics” (DINCOS, CGL2016-78075-P), funded by the Spanish State Plan for Scientific and Technical Research and Innovation. This publication was funded by the Open Access Funding of the TU Dresden Publication Fund.",
year = "2020",
month = jun,
day = "11",
doi = "10.3389/fenvs.2020.00051",
language = "English",
volume = "8",

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TY - JOUR

T1 - Prokaryotic Community Composition and Extracellular Polymeric Substances Affect Soil Microaggregation in Carbonate Containing Semiarid Grasslands

AU - Zethof, Jeroen H.T.

AU - Bettermann, Antje

AU - Vogel, Cordula

AU - Babin, Doreen

AU - Cammeraat, Erik L.H.

AU - Solé-Benet, Albert

AU - Lázaro, Roberto

AU - Luna, Lourdes

AU - Nesme, Joseph

AU - Woche, Susanne K.

AU - Sørensen, Søren J.

AU - Smalla, Kornelia

AU - Kalbitz, Karsten

N1 - Funding information: We thank Stephan Krüger for his mental support and assistance during the sampling campaign, Manuela Unger and Gisela Ciesielski for the laboratory assistance, Tim Schacherl for establishing the microaggregation method and Ilse-Marie Jungkurth for checking the language of the manuscript. Further, we want to thank the Max Planck Institute for Biogeochemistry (Department Biogeochemical Processes, Jena) for the graphitic C measurements. Funding. This study was financially supported by the Deutsche Forschungsgemeinschaft (DFG), Bonn, Germany, under grants KA1737/13-1 and SM 59/18-1 “Extracellular polymeric substances and aggregate stability – how microorganisms affect soil erosion by water.” AS-B, RL, and LL were supported thanks to the Research Project “Biocrust Dynamics” (DINCOS, CGL2016-78075-P), funded by the Spanish State Plan for Scientific and Technical Research and Innovation. This publication was funded by the Open Access Funding of the TU Dresden Publication Fund.

PY - 2020/6/11

Y1 - 2020/6/11

N2 - In the barren semiarid landscape individual plant species improve soil structure, reducing the erosion risks, whereby microaggregates form the most fundamental soil structural components. Extracellular polymeric substances (EPS) are considered an important glue determining aggregation in addition to inorganic binding agents such as carbonates. However, the role of the prokaryotic community in EPS formation and consequently for microaggregation in natural environments is not substantially clarified yet. EPS should be particularly important under semiarid conditions as it forms a protection mechanism of the prokaryotes against desiccation. Therefore, we examined the influence of the prokaryotic community on soil EPS content and subsequently on soil microaggregation in semiarid grasslands, depending on the parent material, common plant species and the distance to the plant. Soil samples were taken over a distance gradient from two major semiarid grassland plant species in Southern Spain, the legume shrub Anthyllis cytisoides and the grass tussock Macrochloa tenacissima, to the surrounding bare soil at two sites, rich and poor in carbonates. Total community DNA and EPS were extracted, followed by quantification of EPS-saccharide, bacterial abundance and examination of the prokaryotic community composition. Further, the particle size distribution of the microaggregate fraction was determined as an indication of microaggregation. We found that the overall prokaryotic community composition differed between the two sites, but not between plant species. Nonetheless, a link between the community composition and EPS content was established, whereby soil organic matter (OM) seems to be a regulating factor as increasing soil OM contents resulted in more EPS-saccharide. Furthermore, microaggregation was enhanced by the canopy, especially at the edge of Macrochloa tussocks. Contrary to the expectation that increasing inorganic C contents would diminish importance of EPS, the parent material richest in inorganic C resulted in a significant effect of EPS-saccharide contents on microaggregation according to the structural equation model. For the inorganic C poor site, EPS-saccharide had no observed direct effect on microaggregation. Based on our results we conclude that the availability of decomposable OM influences the prokaryotic community composition and thereby triggers EPS production whereas large contents of polyvalent cations promote the stabilizing effect of EPS on microaggregates.

AB - In the barren semiarid landscape individual plant species improve soil structure, reducing the erosion risks, whereby microaggregates form the most fundamental soil structural components. Extracellular polymeric substances (EPS) are considered an important glue determining aggregation in addition to inorganic binding agents such as carbonates. However, the role of the prokaryotic community in EPS formation and consequently for microaggregation in natural environments is not substantially clarified yet. EPS should be particularly important under semiarid conditions as it forms a protection mechanism of the prokaryotes against desiccation. Therefore, we examined the influence of the prokaryotic community on soil EPS content and subsequently on soil microaggregation in semiarid grasslands, depending on the parent material, common plant species and the distance to the plant. Soil samples were taken over a distance gradient from two major semiarid grassland plant species in Southern Spain, the legume shrub Anthyllis cytisoides and the grass tussock Macrochloa tenacissima, to the surrounding bare soil at two sites, rich and poor in carbonates. Total community DNA and EPS were extracted, followed by quantification of EPS-saccharide, bacterial abundance and examination of the prokaryotic community composition. Further, the particle size distribution of the microaggregate fraction was determined as an indication of microaggregation. We found that the overall prokaryotic community composition differed between the two sites, but not between plant species. Nonetheless, a link between the community composition and EPS content was established, whereby soil organic matter (OM) seems to be a regulating factor as increasing soil OM contents resulted in more EPS-saccharide. Furthermore, microaggregation was enhanced by the canopy, especially at the edge of Macrochloa tussocks. Contrary to the expectation that increasing inorganic C contents would diminish importance of EPS, the parent material richest in inorganic C resulted in a significant effect of EPS-saccharide contents on microaggregation according to the structural equation model. For the inorganic C poor site, EPS-saccharide had no observed direct effect on microaggregation. Based on our results we conclude that the availability of decomposable OM influences the prokaryotic community composition and thereby triggers EPS production whereas large contents of polyvalent cations promote the stabilizing effect of EPS on microaggregates.

KW - 16S rRNA gene

KW - Anthyllis cytisoides

KW - EPS

KW - Illumina amplicon sequencing

KW - Macrochloa tenacissima

KW - slightly alkaline soils

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JO - Frontiers in Environmental Science

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