Collaborative involvement of woody plant roots and rhizosphere microorganisms in the formation of pedogenetic clays

Frank Reith, William Verboom, John Pate, David Chittleborough

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

BACKGROUND AND AIMS: Previous studies have described the laying down of specific B horizons in south-western Australian ecosystems. This paper presents biomolecular, morphological and physicochemical analyses elucidating the roles of specific woody plant taxa and rhizosphere bacteria in producing these phenomena. METHODS: Clayey deposits within lateral root systems of eucalypts and appropriate background soil samples were collected aseptically at multiple locations on sand dunes flanking Lake Chillinup. Bacterial communities were profiled using tagged next-generation sequencing (Miseq) of the 16S rRNA gene and assigned to operational taxonomic units. Sedimentation, selective dissolution and X-ray diffraction analyses quantitatively identified clay mineral components. Comparisons were made of pedological features between the above eucalypt systems, giant podzols under proteaceous woodland on sand dunes at the study site of Jandakot and apparently similar systems observed elsewhere in the world. KEY RESULTS: Bacterial communities in clay pods are highly diverse, resolving into 569 operational taxonomic units dominated by Actinobacteria at 38.0-87.4 % of the total reads. Multivariate statistical analyses of community fingerprints demonstrated substrate specificity. Differently coloured pods on the same host taxon carry distinctive microfloras correlated to diversities and abundances of Actinobacteria, Acidobacteria, Firmicutes and Proteobacteria. A number of these microbes are known to form biominerals, such as phyllosilicates, carbonates and Fe-oxides. A biogenic origin is suggested for the dominant identified mineral precipitates, namely illite and kaolinite. Comparisons of morphogenetic features of B horizons under eucalypts, tree banksias and other vegetation types show remarkably similar developmental trajectories involving pods of precipitation surrounding specialized fine rootlets and their orderly growth to form a continuous B horizon. CONCLUSIONS: The paper strongly supports the hypothesis that B-horizon development is mediated by highly sophisticated interactions of host plant and rhizosphere organisms in which woody plant taxa govern overall morphogenesis and supply of mineral elements for precipitation, while rhizosphere microorganisms execute biomineralization processes.

Original languageEnglish
Pages (from-to)1007-1018
Number of pages12
JournalAnnals of Botany
Volume124
Issue number6
DOIs
Publication statusPublished - 27 Nov 2019

Fingerprint

B horizons
woody plants
rhizosphere
clay
microorganisms
pods
Actinobacteria
dunes
bacterial communities
minerals
Acidobacteria
Firmicutes
rhizosphere bacteria
illite
Proteobacteria
kaolinite
clay minerals
substrate specificity
X-ray diffraction
vegetation types

Cite this

Reith, Frank ; Verboom, William ; Pate, John ; Chittleborough, David. / Collaborative involvement of woody plant roots and rhizosphere microorganisms in the formation of pedogenetic clays. In: Annals of Botany. 2019 ; Vol. 124, No. 6. pp. 1007-1018.
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abstract = "BACKGROUND AND AIMS: Previous studies have described the laying down of specific B horizons in south-western Australian ecosystems. This paper presents biomolecular, morphological and physicochemical analyses elucidating the roles of specific woody plant taxa and rhizosphere bacteria in producing these phenomena. METHODS: Clayey deposits within lateral root systems of eucalypts and appropriate background soil samples were collected aseptically at multiple locations on sand dunes flanking Lake Chillinup. Bacterial communities were profiled using tagged next-generation sequencing (Miseq) of the 16S rRNA gene and assigned to operational taxonomic units. Sedimentation, selective dissolution and X-ray diffraction analyses quantitatively identified clay mineral components. Comparisons were made of pedological features between the above eucalypt systems, giant podzols under proteaceous woodland on sand dunes at the study site of Jandakot and apparently similar systems observed elsewhere in the world. KEY RESULTS: Bacterial communities in clay pods are highly diverse, resolving into 569 operational taxonomic units dominated by Actinobacteria at 38.0-87.4 {\%} of the total reads. Multivariate statistical analyses of community fingerprints demonstrated substrate specificity. Differently coloured pods on the same host taxon carry distinctive microfloras correlated to diversities and abundances of Actinobacteria, Acidobacteria, Firmicutes and Proteobacteria. A number of these microbes are known to form biominerals, such as phyllosilicates, carbonates and Fe-oxides. A biogenic origin is suggested for the dominant identified mineral precipitates, namely illite and kaolinite. Comparisons of morphogenetic features of B horizons under eucalypts, tree banksias and other vegetation types show remarkably similar developmental trajectories involving pods of precipitation surrounding specialized fine rootlets and their orderly growth to form a continuous B horizon. CONCLUSIONS: The paper strongly supports the hypothesis that B-horizon development is mediated by highly sophisticated interactions of host plant and rhizosphere organisms in which woody plant taxa govern overall morphogenesis and supply of mineral elements for precipitation, while rhizosphere microorganisms execute biomineralization processes.",
keywords = "Actinobacteria, B horizon formation, banksias, biomineralization, element mining, Eucalypts, hydraulic lift, niche construction, pedogenetic clays, Phytotarium, rhizosphere microbiome, root morphology",
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Collaborative involvement of woody plant roots and rhizosphere microorganisms in the formation of pedogenetic clays. / Reith, Frank; Verboom, William; Pate, John; Chittleborough, David.

In: Annals of Botany, Vol. 124, No. 6, 27.11.2019, p. 1007-1018.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Collaborative involvement of woody plant roots and rhizosphere microorganisms in the formation of pedogenetic clays

AU - Reith, Frank

AU - Verboom, William

AU - Pate, John

AU - Chittleborough, David

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N2 - BACKGROUND AND AIMS: Previous studies have described the laying down of specific B horizons in south-western Australian ecosystems. This paper presents biomolecular, morphological and physicochemical analyses elucidating the roles of specific woody plant taxa and rhizosphere bacteria in producing these phenomena. METHODS: Clayey deposits within lateral root systems of eucalypts and appropriate background soil samples were collected aseptically at multiple locations on sand dunes flanking Lake Chillinup. Bacterial communities were profiled using tagged next-generation sequencing (Miseq) of the 16S rRNA gene and assigned to operational taxonomic units. Sedimentation, selective dissolution and X-ray diffraction analyses quantitatively identified clay mineral components. Comparisons were made of pedological features between the above eucalypt systems, giant podzols under proteaceous woodland on sand dunes at the study site of Jandakot and apparently similar systems observed elsewhere in the world. KEY RESULTS: Bacterial communities in clay pods are highly diverse, resolving into 569 operational taxonomic units dominated by Actinobacteria at 38.0-87.4 % of the total reads. Multivariate statistical analyses of community fingerprints demonstrated substrate specificity. Differently coloured pods on the same host taxon carry distinctive microfloras correlated to diversities and abundances of Actinobacteria, Acidobacteria, Firmicutes and Proteobacteria. A number of these microbes are known to form biominerals, such as phyllosilicates, carbonates and Fe-oxides. A biogenic origin is suggested for the dominant identified mineral precipitates, namely illite and kaolinite. Comparisons of morphogenetic features of B horizons under eucalypts, tree banksias and other vegetation types show remarkably similar developmental trajectories involving pods of precipitation surrounding specialized fine rootlets and their orderly growth to form a continuous B horizon. CONCLUSIONS: The paper strongly supports the hypothesis that B-horizon development is mediated by highly sophisticated interactions of host plant and rhizosphere organisms in which woody plant taxa govern overall morphogenesis and supply of mineral elements for precipitation, while rhizosphere microorganisms execute biomineralization processes.

AB - BACKGROUND AND AIMS: Previous studies have described the laying down of specific B horizons in south-western Australian ecosystems. This paper presents biomolecular, morphological and physicochemical analyses elucidating the roles of specific woody plant taxa and rhizosphere bacteria in producing these phenomena. METHODS: Clayey deposits within lateral root systems of eucalypts and appropriate background soil samples were collected aseptically at multiple locations on sand dunes flanking Lake Chillinup. Bacterial communities were profiled using tagged next-generation sequencing (Miseq) of the 16S rRNA gene and assigned to operational taxonomic units. Sedimentation, selective dissolution and X-ray diffraction analyses quantitatively identified clay mineral components. Comparisons were made of pedological features between the above eucalypt systems, giant podzols under proteaceous woodland on sand dunes at the study site of Jandakot and apparently similar systems observed elsewhere in the world. KEY RESULTS: Bacterial communities in clay pods are highly diverse, resolving into 569 operational taxonomic units dominated by Actinobacteria at 38.0-87.4 % of the total reads. Multivariate statistical analyses of community fingerprints demonstrated substrate specificity. Differently coloured pods on the same host taxon carry distinctive microfloras correlated to diversities and abundances of Actinobacteria, Acidobacteria, Firmicutes and Proteobacteria. A number of these microbes are known to form biominerals, such as phyllosilicates, carbonates and Fe-oxides. A biogenic origin is suggested for the dominant identified mineral precipitates, namely illite and kaolinite. Comparisons of morphogenetic features of B horizons under eucalypts, tree banksias and other vegetation types show remarkably similar developmental trajectories involving pods of precipitation surrounding specialized fine rootlets and their orderly growth to form a continuous B horizon. CONCLUSIONS: The paper strongly supports the hypothesis that B-horizon development is mediated by highly sophisticated interactions of host plant and rhizosphere organisms in which woody plant taxa govern overall morphogenesis and supply of mineral elements for precipitation, while rhizosphere microorganisms execute biomineralization processes.

KW - Actinobacteria

KW - B horizon formation

KW - banksias

KW - biomineralization

KW - element mining

KW - Eucalypts

KW - hydraulic lift

KW - niche construction

KW - pedogenetic clays

KW - Phytotarium

KW - rhizosphere microbiome

KW - root morphology

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DO - 10.1093/aob/mcz065

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JO - Annals of Botany

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