Abstract
We assessed the effects of EDTA and selected plant growth-promoting rhizobacteria (PGPR) on the phytoremediation of soils and sediments historically contaminated by Cr, Ni, and Cu. A total of 42 bacterial strains resistant to these heavy metals (HMs) were isolated and screened for PGP traits and metal bioaccumulation, and two Enterobacter spp. strains were finally selected. Phytoremediation pot experiments of 2 months duration were carried out with hemp ( Cannabis sativa L.) and giant reed ( Arundo donax L.) grown on soils and sediments respectively, comparing in both cases the effects of bioaugmentation with a single PGPR and EDTA addition on plant and root growth, plant HM uptake, HM leaching, as well as the changes that occurred in soil microbial communities (structure, biomass, and activity). Good removal percentages on a dry mass basis of Cr (0.4%), Ni (0.6%), and Cu (0.9%) were observed in giant reed while negligible values (<100‰) in hemp. In giant reed, HMs accumulated differentially in plant (rhizomes > > roots > leaves > stems) with largest quantities in rhizomes (Cr 0.6, Ni 3.7, and Cu 2.2 g plant –1 ). EDTA increased Ni and Cu translocation to aerial parts in both crops, despite that in sediments high HM concentrations in leachates were measured. PGPR did not impact fine root diameter distribution of both crops compared with control while EDTA negatively affected root diameter class length (DCL) distribution. Under HM contamination, giant reed roots become shorter (from 5.2 to 2.3 mm cm –3 ) while hemp roots become shorter and thickened from 0.13 to 0.26 mm. A consistent indirect effect of HM levels on the soil microbiome (diversity and activity) mediated by plant response (root DCL distribution) was observed. Multivariate analysis of bacterial diversity and activity revealed not only significant effects of plant and soil type (rhizosphere vs. bulk) but also a clear and similar differentiation of communities between control, EDTA, and PGPR treatments. We propose root DCL distribution as a key plant trait to understand detrimental effect of HMs on microbial communities. Positive evidence of the soil-microbe-plant interactions occurring when bioaugmentation with PGPR is associated with deep-rooting perennial crops makes this combination preferable over the one with chelating agents. Such knowledge might help to yield better bioaugmented bioremediation results in contaminated sites.
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Claims 20
Claim · model-written summary
Giant reed removed 0.4% of Cr on a dry mass basis.
- Taxon
- giant reed
Arundo donaxe1
- Outcome
- removal percentages on a dry mass basise1
- Value
- 0.4%e1
- Qualifier
- Cre1
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e1“Good removal percentages on a dry mass basis of Cr (0.4%), Ni (0.6%), and Cu (0.9%) were observed in giant reed”
Claim · model-written summary
Giant reed removed 0.6% of Ni on a dry mass basis.
- Taxon
- giant reed
Arundo donaxe1
- Outcome
- removal percentages on a dry mass basise1
- Value
- 0.6%e1
- Qualifier
- Nie1
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e1“Good removal percentages on a dry mass basis of Cr (0.4%), Ni (0.6%), and Cu (0.9%) were observed in giant reed”
Claim · model-written summary
Giant reed removed 0.9% of Cu on a dry mass basis.
- Taxon
- giant reed
Arundo donaxe1
- Outcome
- removal percentages on a dry mass basise1
- Value
- 0.9%e1
- Qualifier
- Cue1
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e1“Good removal percentages on a dry mass basis of Cr (0.4%), Ni (0.6%), and Cu (0.9%) were observed in giant reed”
Claim · model-written summary
Hemp removal of metals was negligible, below 100‰.
- Taxon
- hemp
Cannabis sativa subsp. sativae3 - Outcome
- valuese2
- Value
- <100‰e2
- Qualifier
- negligiblee2
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e2“negligible values (<100‰) in hemp”
e3“Phytoremediation pot experiments of 2 months duration were carried out with hemp ( Cannabis sativa L. ) and giant reed ( Arundo donax L. )”
Claim · model-written summary
Heavy metals accumulated differentially in giant reed plants, with the order rhizomes > roots > leaves > stems.
- Taxon
- giant reed
Arundo donaxe4
- Organ / stage
- rhizomes > > roots > leaves > stemse4
- Outcome
- HMs accumulated differentially in plante4
Not reportedDirection
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e4“In giant reed, HMs accumulated differentially in plant (rhizomes > > roots > leaves > stems)”
Claim · model-written summary
The largest Cr quantity in giant reed was in the rhizomes, at 0.6.
- Taxon
- giant reed
Arundo donaxe4
- Organ / stage
- rhizomese5
- Outcome
- largest quantitiese5
- Value
- 0.6e5
- Qualifier
- Cre5
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e4“In giant reed, HMs accumulated differentially in plant (rhizomes > > roots > leaves > stems)”
e5“with largest quantities in rhizomes (Cr 0.6, Ni 3.7, and Cu 2.2 g plant –1 )”
Claim · model-written summary
The largest Ni quantity in giant reed was in the rhizomes, at 3.7.
- Taxon
- giant reed
Arundo donaxe4
- Organ / stage
- rhizomese5
- Outcome
- largest quantitiese5
- Value
- 3.7e5
- Qualifier
- Nie5
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e4“In giant reed, HMs accumulated differentially in plant (rhizomes > > roots > leaves > stems)”
e5“with largest quantities in rhizomes (Cr 0.6, Ni 3.7, and Cu 2.2 g plant –1 )”
Claim · model-written summary
The largest Cu quantity in giant reed was in the rhizomes, at 2.2 g plant –1.
- Taxon
- giant reed
Arundo donaxe4
- Organ / stage
- rhizomese5
- Outcome
- largest quantitiese5
- Value
- 2.2 g plant –1e5
- Qualifier
- Cue5
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e4“In giant reed, HMs accumulated differentially in plant (rhizomes > > roots > leaves > stems)”
e5“with largest quantities in rhizomes (Cr 0.6, Ni 3.7, and Cu 2.2 g plant –1 )”
Claim · model-written summary
EDTA increased Ni and Cu translocation to the aerial parts of hemp and giant reed.
- Taxon
- hemp
Cannabis sativa subsp. sativae3 - Treatment
- EDTAe6
- Outcome
- Ni and Cu translocation to aerial partse6
- Direction
- increasede6
- Qualifier
- in both cropse6
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e3“Phytoremediation pot experiments of 2 months duration were carried out with hemp ( Cannabis sativa L. ) and giant reed ( Arundo donax L. )”
e6“EDTA increased Ni and Cu translocation to aerial parts in both crops”
Claim · model-written summary
Sediments had high HM concentrations in leachates.
- Taxon
- giant reed
Arundo donaxe4
- Outcome
- HM concentrations in leachatese7
- Qualifier
- highe7
- Setting
- sedimentse7
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e4“In giant reed, HMs accumulated differentially in plant (rhizomes > > roots > leaves > stems)”
e7“in sediments high HM concentrations in leachates were measured”
Claim · model-written summary
PGPR did not change the fine root diameter distribution of hemp compared with the control.
- Taxon
- hemp
Cannabis sativa subsp. sativae3 - Treatment
- PGPRe0
- Outcome
- fine root diameter distributione0
- Direction
- did not impacte0
- Qualifier
- both cropse0
- Comparator
- controle0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e3“Phytoremediation pot experiments of 2 months duration were carried out with hemp ( Cannabis sativa L. ) and giant reed ( Arundo donax L. )”
e0“PGPR did not impact fine root diameter distribution of both crops compared with control”
Claim · model-written summary
EDTA negatively affected the root diameter class length distribution of hemp.
- Taxon
- hemp
Cannabis sativa subsp. sativae3 - Treatment
- EDTAe0
- Outcome
- root diameter class length (DCL) distributione0
- Direction
- negatively affectede0
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e3“Phytoremediation pot experiments of 2 months duration were carried out with hemp ( Cannabis sativa L. ) and giant reed ( Arundo donax L. )”
e0“EDTA negatively affected root diameter class length (DCL) distribution”
Claim · model-written summary
Under HM contamination, giant reed roots became shorter, from 5.2 to 2.3 mm cm –3.
- Taxon
- giant reed
Arundo donaxe0
- Treatment
- HM contaminatione0
- Outcome
- giant reed rootse0
- Direction
- shortere0
- Value
- 5.2 to 2.3 mm cm –3e0
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“Under HM contamination, giant reed roots become shorter (from 5.2 to 2.3 mm cm –3 )”
Claim · model-written summary
Under HM contamination, hemp roots became shorter.
- Taxon
- hemp
Cannabis sativa subsp. sativae2 - Treatment
- HM contaminatione0
- Outcome
- hemp rootse2
- Direction
- shortere2
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e0“Under HM contamination, giant reed roots become shorter (from 5.2 to 2.3 mm cm –3 )”
e2“hemp roots become shorter and thickened from 0.13 to 0.26 mm”
Claim · model-written summary
Under HM contamination, hemp roots became thicker, from 0.13 to 0.26 mm.
- Taxon
- hemp
Cannabis sativa subsp. sativae2 - Treatment
- HM contaminatione0
- Outcome
- hemp rootse2
- Direction
- thickenede2
- Value
- 0.13 to 0.26 mme2
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e0“Under HM contamination, giant reed roots become shorter (from 5.2 to 2.3 mm cm –3 )”
e2“hemp roots become shorter and thickened from 0.13 to 0.26 mm”
Claim · model-written summary
HM levels indirectly affected the soil microbiome (diversity and activity), mediated by the root DCL distribution of hemp.
- Taxon
- hemp
Cannabis sativa subsp. sativae3 - Treatment
- HM levelse0
- Outcome
- soil microbiome (diversity and activity)e0
- Qualifier
- mediated by plant response (root DCL distribution)e0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e3“Phytoremediation pot experiments of 2 months duration were carried out with hemp ( Cannabis sativa L. ) and giant reed ( Arundo donax L. )”
e0“A consistent indirect effect of HM levels on the soil microbiome (diversity and activity) mediated by plant response (root DCL distribution) was observed”
Claim · model-written summary
Bacterial diversity and activity differed significantly with plant and soil type (rhizosphere vs. bulk).
- Taxon
- hemp
Cannabis sativa subsp. sativae3 - Treatment
- plant and soil type (rhizosphere vs. bulk)e0
- Outcome
- bacterial diversity and activitye0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e3“Phytoremediation pot experiments of 2 months duration were carried out with hemp ( Cannabis sativa L. ) and giant reed ( Arundo donax L. )”
e0“Multivariate analysis of bacterial diversity and activity revealed not only significant effects of plant and soil type (rhizosphere vs. bulk)”
Claim · model-written summary
Bacterial communities differentiated clearly between the control, EDTA and PGPR treatments.
- Taxon
- hemp
Cannabis sativa subsp. sativae3 - Treatment
- EDTA, and PGPR treatmentse0
- Outcome
- differentiation of communitiese0
- Comparator
- controle0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e3“Phytoremediation pot experiments of 2 months duration were carried out with hemp ( Cannabis sativa L. ) and giant reed ( Arundo donax L. )”
e0“clear and similar differentiation of communities between control, EDTA, and PGPR treatments”
Claim · model-written summary
The authors propose root DCL distribution as a key plant trait for understanding the detrimental effect of HMs on microbial communities.
- Taxon
- hemp
Cannabis sativa subsp. sativae3 - Outcome
- root DCL distribution as a key plant traite0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Verbatim
e3“Phytoremediation pot experiments of 2 months duration were carried out with hemp ( Cannabis sativa L. ) and giant reed ( Arundo donax L. )”
e0“We propose root DCL distribution as a key plant trait to understand detrimental effect of HMs on microbial communities”
Claim · model-written summary
The authors recommend bioaugmentation with PGPR over chelating agents for deep-rooting perennial crops.
Verbatim
e0“Positive evidence of the soil-microbe-plant interactions occurring when bioaugmentation with PGPR is associated with deep-rooting perennial crops makes this combination preferable over the one with chelating agents”
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