Can Phytoremediation-Induced Changes in the Microbiome Improve Saline/Sodic Soil and Plant Health?

Increasing soil salinity and/or sodicity is an expanding problem in the Northern Great Plains (NGP) of North America. This study investigated the impact of phytoremediation on the soil microbiome and if changes, in turn, had positive or negative effects on plant establishment. Amplicon sequencing an...

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Main Authors: Achal Neupane, Duncan Jakubowski, Douglas Fiedler, Liping Gu, Sharon A. Clay, David E. Clay, Shin-Yi Lee Marzano
Format: Article
Language:English
Published: MDPI AG 2023-12-01
Series:Agronomy
Subjects:
Online Access:https://www.mdpi.com/2073-4395/14/1/29
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author Achal Neupane
Duncan Jakubowski
Douglas Fiedler
Liping Gu
Sharon A. Clay
David E. Clay
Shin-Yi Lee Marzano
author_facet Achal Neupane
Duncan Jakubowski
Douglas Fiedler
Liping Gu
Sharon A. Clay
David E. Clay
Shin-Yi Lee Marzano
author_sort Achal Neupane
collection DOAJ
description Increasing soil salinity and/or sodicity is an expanding problem in the Northern Great Plains (NGP) of North America. This study investigated the impact of phytoremediation on the soil microbiome and if changes, in turn, had positive or negative effects on plant establishment. Amplicon sequencing and gas chromatograph/mass spectrometer analysis compared root metabolites and microbial composition of bulk vs. rhizosphere soils between two soil types (productive and saline/sodic). Beta-diversity analysis indicated that bacterial and fungal communities from both the bulk and rhizosphere soils from each soil type clustered separately, indicating dissimilar microbial composition. Plant species also influenced both root-associated bacterial and fungal communities with separate clustering of operational taxonomic units (OTUs) identified. Canonical correlation analysis (CCA) found a clear association between specific soil characteristics and soil types. Bacterial and fungal OTUs from productive soil were correlated with greater %Ca Sat, %H Sat, and potassium (ppm), especially for OTUs differentially enriched in productive soil. Both bacterial and fungal OTUs from saline/sodic soil are associated with increased Ca (ppm), soil pH, %Na Sat and CEC. Metabolite analysis showed that kochia (<i>Bassia scoparia</i>) roots from the saline/sodic soil had a 4.4-fold decrease in pantothenate accumulation (<i>p</i> = 0.004). Moreover, two endophytic bacterial isolates, a <i>Bacillus</i> spp. and a previously uncultured halophile, isolated from creeping foxtail (<i>Alopecurus arundinaceus)</i> grown in saline/sodic soil and used as buckwheat (<i>Fagopyrum esculentum</i>) seed inoculants, significantly increased seed germination by >30% and vigor index by 0.2 under osmotic stress (0.2 M NaCl) (<i>p</i> < 0.05). This study revealed the importance of soil, root-associated, and endophytic microbiomes. Using native microbes as seed inoculants may help in establishment and growth of species used for phytoremediation of saline/sodic soil.
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spelling doaj.art-1741a76eb6364380a70d33cd3a25845c2024-01-26T14:21:28ZengMDPI AGAgronomy2073-43952023-12-011412910.3390/agronomy14010029Can Phytoremediation-Induced Changes in the Microbiome Improve Saline/Sodic Soil and Plant Health?Achal Neupane0Duncan Jakubowski1Douglas Fiedler2Liping Gu3Sharon A. Clay4David E. Clay5Shin-Yi Lee Marzano6Department of Biology and Microbiology, South Dakota State University, Brookings, SD 57007, USADepartment of Biology and Microbiology, South Dakota State University, Brookings, SD 57007, USADepartment of Agronomy, Horticulture, and Plant Science, South Dakota State University, Brookings, SD 57007, USADepartment of Biology and Microbiology, South Dakota State University, Brookings, SD 57007, USADepartment of Agronomy, Horticulture, and Plant Science, South Dakota State University, Brookings, SD 57007, USADepartment of Agronomy, Horticulture, and Plant Science, South Dakota State University, Brookings, SD 57007, USADepartment of Biology and Microbiology, South Dakota State University, Brookings, SD 57007, USAIncreasing soil salinity and/or sodicity is an expanding problem in the Northern Great Plains (NGP) of North America. This study investigated the impact of phytoremediation on the soil microbiome and if changes, in turn, had positive or negative effects on plant establishment. Amplicon sequencing and gas chromatograph/mass spectrometer analysis compared root metabolites and microbial composition of bulk vs. rhizosphere soils between two soil types (productive and saline/sodic). Beta-diversity analysis indicated that bacterial and fungal communities from both the bulk and rhizosphere soils from each soil type clustered separately, indicating dissimilar microbial composition. Plant species also influenced both root-associated bacterial and fungal communities with separate clustering of operational taxonomic units (OTUs) identified. Canonical correlation analysis (CCA) found a clear association between specific soil characteristics and soil types. Bacterial and fungal OTUs from productive soil were correlated with greater %Ca Sat, %H Sat, and potassium (ppm), especially for OTUs differentially enriched in productive soil. Both bacterial and fungal OTUs from saline/sodic soil are associated with increased Ca (ppm), soil pH, %Na Sat and CEC. Metabolite analysis showed that kochia (<i>Bassia scoparia</i>) roots from the saline/sodic soil had a 4.4-fold decrease in pantothenate accumulation (<i>p</i> = 0.004). Moreover, two endophytic bacterial isolates, a <i>Bacillus</i> spp. and a previously uncultured halophile, isolated from creeping foxtail (<i>Alopecurus arundinaceus)</i> grown in saline/sodic soil and used as buckwheat (<i>Fagopyrum esculentum</i>) seed inoculants, significantly increased seed germination by >30% and vigor index by 0.2 under osmotic stress (0.2 M NaCl) (<i>p</i> < 0.05). This study revealed the importance of soil, root-associated, and endophytic microbiomes. Using native microbes as seed inoculants may help in establishment and growth of species used for phytoremediation of saline/sodic soil.https://www.mdpi.com/2073-4395/14/1/29phytoremediationsaline/sodic soilmicrobiomemetaboliteseed inoculum
spellingShingle Achal Neupane
Duncan Jakubowski
Douglas Fiedler
Liping Gu
Sharon A. Clay
David E. Clay
Shin-Yi Lee Marzano
Can Phytoremediation-Induced Changes in the Microbiome Improve Saline/Sodic Soil and Plant Health?
Agronomy
phytoremediation
saline/sodic soil
microbiome
metabolite
seed inoculum
title Can Phytoremediation-Induced Changes in the Microbiome Improve Saline/Sodic Soil and Plant Health?
title_full Can Phytoremediation-Induced Changes in the Microbiome Improve Saline/Sodic Soil and Plant Health?
title_fullStr Can Phytoremediation-Induced Changes in the Microbiome Improve Saline/Sodic Soil and Plant Health?
title_full_unstemmed Can Phytoremediation-Induced Changes in the Microbiome Improve Saline/Sodic Soil and Plant Health?
title_short Can Phytoremediation-Induced Changes in the Microbiome Improve Saline/Sodic Soil and Plant Health?
title_sort can phytoremediation induced changes in the microbiome improve saline sodic soil and plant health
topic phytoremediation
saline/sodic soil
microbiome
metabolite
seed inoculum
url https://www.mdpi.com/2073-4395/14/1/29
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