Rhizoplane Bacteria and Plant Species Co-determine Phosphorus-Mediated Microbial Legacy Effect
Much effort has been directed toward increasing the availability of soil residual phosphorus (P). However, little information is available for the P fertilization-induced biotic P legacy and its mediation of plant P uptake. We collected microbial inocula from a monoculture maize field site with a 10...
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Published in | Frontiers in microbiology Vol. 10; p. 2856 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
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10.12.2019
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Abstract | Much effort has been directed toward increasing the availability of soil residual phosphorus (P). However, little information is available for the P fertilization-induced biotic P legacy and its mediation of plant P uptake. We collected microbial inocula from a monoculture maize field site with a 10-year P-fertilization history. A greenhouse experiment was conducted to investigate whether bacterial communities, as a result of different P-fertilization history (nil P, 33 and/or 131 kg P kg ha
yr
), affected the growth of a conspecific (maize) or heterospecific (clover) plant, at two levels of current P application (5 and 30 mg P kg
soil; P
and P
). Deep amplicon sequencing (16S rRNA) was used to determine the maize and clover root-associated bacterial microbiome in different rhizocompartments (rhizoplane, rhizosphere, bulk soil). For both maize and clover, rhizocompartment and host identity were the dominant factors shaping bacterial assemblages, followed by P supply level and the inoculum effect was smallest. Bacterial operational taxonomic unit (OTU) numbers decreased from bulk soil to rhizoplane, whilst specific OTUs were enriched from bulk soil to rhizoplane. A clear hierarchical habitat filtering of bacterial communities was observed in the rhizoplane of the two plant species. The functional prediction of dominant bacterial taxa in the rhizoplane differed between clover and maize, and clover microbiota were more closely associated with P metabolism and maize with carbon cycling. More connected and complex interactions were observed in the clover rhizoplane compared to maize. The microbial legacy effect caused by long-term P fertilization is overridden by host identity and rhizocompartment. Our results highlight the importance of crop diversification in improving P efficiency. The fine-tuning of rhizosphere microbiome in host metabolism indicates that the functions of microbial communities should be integrated into P management to increase P use efficiency and sustainable food production. |
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AbstractList | Much effort has been directed toward increasing the availability of soil residual phosphorus (P). However, little information is available for the P fertilization-induced biotic P legacy and its mediation of plant P uptake. We collected microbial inocula from a monoculture maize field site with a 10-year P-fertilization history. A greenhouse experiment was conducted to investigate whether bacterial communities, as a result of different P-fertilization history (nil P, 33 and/or 131 kg P kg ha
–1
yr
–1
), affected the growth of a conspecific (maize) or heterospecific (clover) plant, at two levels of current P application (5 and 30 mg P kg
–1
soil; P
5
and P
30
). Deep amplicon sequencing (16S rRNA) was used to determine the maize and clover root-associated bacterial microbiome in different rhizocompartments (rhizoplane, rhizosphere, bulk soil). For both maize and clover, rhizocompartment and host identity were the dominant factors shaping bacterial assemblages, followed by P supply level and the inoculum effect was smallest. Bacterial operational taxonomic unit (OTU) numbers decreased from bulk soil to rhizoplane, whilst specific OTUs were enriched from bulk soil to rhizoplane. A clear hierarchical habitat filtering of bacterial communities was observed in the rhizoplane of the two plant species. The functional prediction of dominant bacterial taxa in the rhizoplane differed between clover and maize, and clover microbiota were more closely associated with P metabolism and maize with carbon cycling. More connected and complex interactions were observed in the clover rhizoplane compared to maize. The microbial legacy effect caused by long-term P fertilization is overridden by host identity and rhizocompartment. Our results highlight the importance of crop diversification in improving P efficiency. The fine-tuning of rhizosphere microbiome in host metabolism indicates that the functions of microbial communities should be integrated into P management to increase P use efficiency and sustainable food production. Much effort has been directed toward increasing the availability of soil residual phosphorus (P). However, little information is available for the P fertilization-induced biotic P legacy and its mediation of plant P uptake. We collected microbial inocula from a monoculture maize field site with a 10-year P-fertilization history. A greenhouse experiment was conducted to investigate whether bacterial communities, as a result of different P-fertilization history (nil P, 33 and/or 131 kg P kg ha–1 yr–1), affected the growth of a conspecific (maize) or heterospecific (clover) plant, at two levels of current P application (5 and 30 mg P kg–1 soil; P5 and P30). Deep amplicon sequencing (16S rRNA) was used to determine the maize and clover root-associated bacterial microbiome in different rhizocompartments (rhizoplane, rhizosphere, bulk soil). For both maize and clover, rhizocompartment and host identity were the dominant factors shaping bacterial assemblages, followed by P supply level and the inoculum effect was smallest. Bacterial operational taxonomic unit (OTU) numbers decreased from bulk soil to rhizoplane, whilst specific OTUs were enriched from bulk soil to rhizoplane. A clear hierarchical habitat filtering of bacterial communities was observed in the rhizoplane of the two plant species. The functional prediction of dominant bacterial taxa in the rhizoplane differed between clover and maize, and clover microbiota were more closely associated with P metabolism and maize with carbon cycling. More connected and complex interactions were observed in the clover rhizoplane compared to maize. The microbial legacy effect caused by long-term P fertilization is overridden by host identity and rhizocompartment. Our results highlight the importance of crop diversification in improving P efficiency. The fine-tuning of rhizosphere microbiome in host metabolism indicates that the functions of microbial communities should be integrated into P management to increase P use efficiency and sustainable food production. Much effort has been directed toward increasing the availability of soil residual phosphorus (P). However, little information is available for the P fertilization-induced biotic P legacy and its mediation of plant P uptake. We collected microbial inocula from a monoculture maize field site with a 10-year P-fertilization history. A greenhouse experiment was conducted to investigate whether bacterial communities, as a result of different P-fertilization history (nil P, 33 and/or 131 kg P kg ha yr ), affected the growth of a conspecific (maize) or heterospecific (clover) plant, at two levels of current P application (5 and 30 mg P kg soil; P and P ). Deep amplicon sequencing (16S rRNA) was used to determine the maize and clover root-associated bacterial microbiome in different rhizocompartments (rhizoplane, rhizosphere, bulk soil). For both maize and clover, rhizocompartment and host identity were the dominant factors shaping bacterial assemblages, followed by P supply level and the inoculum effect was smallest. Bacterial operational taxonomic unit (OTU) numbers decreased from bulk soil to rhizoplane, whilst specific OTUs were enriched from bulk soil to rhizoplane. A clear hierarchical habitat filtering of bacterial communities was observed in the rhizoplane of the two plant species. The functional prediction of dominant bacterial taxa in the rhizoplane differed between clover and maize, and clover microbiota were more closely associated with P metabolism and maize with carbon cycling. More connected and complex interactions were observed in the clover rhizoplane compared to maize. The microbial legacy effect caused by long-term P fertilization is overridden by host identity and rhizocompartment. Our results highlight the importance of crop diversification in improving P efficiency. The fine-tuning of rhizosphere microbiome in host metabolism indicates that the functions of microbial communities should be integrated into P management to increase P use efficiency and sustainable food production. Much effort has been directed toward increasing the availability of soil residual phosphorus (P). However, little information is available for the P fertilization-induced biotic P legacy and its mediation of plant P uptake. We collected microbial inocula from a monoculture maize field site with a 10-year P-fertilization history. A greenhouse experiment was conducted to investigate whether bacterial communities, as a result of different P-fertilization history (nil P, 33 and/or 131 kg P kg ha-1 yr-1), affected the growth of a conspecific (maize) or heterospecific (clover) plant, at two levels of current P application (5 and 30 mg P kg-1 soil; P5 and P30). Deep amplicon sequencing (16S rRNA) was used to determine the maize and clover root-associated bacterial microbiome in different rhizocompartments (rhizoplane, rhizosphere, bulk soil). For both maize and clover, rhizocompartment and host identity were the dominant factors shaping bacterial assemblages, followed by P supply level and the inoculum effect was smallest. Bacterial operational taxonomic unit (OTU) numbers decreased from bulk soil to rhizoplane, whilst specific OTUs were enriched from bulk soil to rhizoplane. A clear hierarchical habitat filtering of bacterial communities was observed in the rhizoplane of the two plant species. The functional prediction of dominant bacterial taxa in the rhizoplane differed between clover and maize, and clover microbiota were more closely associated with P metabolism and maize with carbon cycling. More connected and complex interactions were observed in the clover rhizoplane compared to maize. The microbial legacy effect caused by long-term P fertilization is overridden by host identity and rhizocompartment. Our results highlight the importance of crop diversification in improving P efficiency. The fine-tuning of rhizosphere microbiome in host metabolism indicates that the functions of microbial communities should be integrated into P management to increase P use efficiency and sustainable food production.Much effort has been directed toward increasing the availability of soil residual phosphorus (P). However, little information is available for the P fertilization-induced biotic P legacy and its mediation of plant P uptake. We collected microbial inocula from a monoculture maize field site with a 10-year P-fertilization history. A greenhouse experiment was conducted to investigate whether bacterial communities, as a result of different P-fertilization history (nil P, 33 and/or 131 kg P kg ha-1 yr-1), affected the growth of a conspecific (maize) or heterospecific (clover) plant, at two levels of current P application (5 and 30 mg P kg-1 soil; P5 and P30). Deep amplicon sequencing (16S rRNA) was used to determine the maize and clover root-associated bacterial microbiome in different rhizocompartments (rhizoplane, rhizosphere, bulk soil). For both maize and clover, rhizocompartment and host identity were the dominant factors shaping bacterial assemblages, followed by P supply level and the inoculum effect was smallest. Bacterial operational taxonomic unit (OTU) numbers decreased from bulk soil to rhizoplane, whilst specific OTUs were enriched from bulk soil to rhizoplane. A clear hierarchical habitat filtering of bacterial communities was observed in the rhizoplane of the two plant species. The functional prediction of dominant bacterial taxa in the rhizoplane differed between clover and maize, and clover microbiota were more closely associated with P metabolism and maize with carbon cycling. More connected and complex interactions were observed in the clover rhizoplane compared to maize. The microbial legacy effect caused by long-term P fertilization is overridden by host identity and rhizocompartment. Our results highlight the importance of crop diversification in improving P efficiency. The fine-tuning of rhizosphere microbiome in host metabolism indicates that the functions of microbial communities should be integrated into P management to increase P use efficiency and sustainable food production. |
Author | Bei, Shuikuan Zhang, Junling Lang, Ming Kuyper, Thomas W. Li, Xia |
AuthorAffiliation | 3 Key Laboratory of Plant-Soil Interactions, Ministry of Education , Beijing , China 4 School of Life Science, Shanxi Datong University , Datong , China 1 College of Resources and Environment, Southwest University , Chongqing , China 5 Soil Biology Group, Wageningen University , Wageningen , Netherlands 2 Centre for Resources, Environment and Food Security, College of Resources and Environmental Sciences, China Agricultural University , Beijing , China |
AuthorAffiliation_xml | – name: 2 Centre for Resources, Environment and Food Security, College of Resources and Environmental Sciences, China Agricultural University , Beijing , China – name: 3 Key Laboratory of Plant-Soil Interactions, Ministry of Education , Beijing , China – name: 4 School of Life Science, Shanxi Datong University , Datong , China – name: 1 College of Resources and Environment, Southwest University , Chongqing , China – name: 5 Soil Biology Group, Wageningen University , Wageningen , Netherlands |
Author_xml | – sequence: 1 givenname: Ming surname: Lang fullname: Lang, Ming – sequence: 2 givenname: Shuikuan surname: Bei fullname: Bei, Shuikuan – sequence: 3 givenname: Xia surname: Li fullname: Li, Xia – sequence: 4 givenname: Thomas W. surname: Kuyper fullname: Kuyper, Thomas W. – sequence: 5 givenname: Junling surname: Zhang fullname: Zhang, Junling |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31921037$$D View this record in MEDLINE/PubMed |
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ContentType | Journal Article |
Copyright | Copyright © 2019 Lang, Bei, Li, Kuyper and Zhang. Copyright © 2019 Lang, Bei, Li, Kuyper and Zhang. 2019 Lang, Bei, Li, Kuyper and Zhang |
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Keywords | rhizocompartment microbial ecological network long-term phosphorus fertilization high-throughput sequencing soil microbiome |
Language | English |
License | Copyright © 2019 Lang, Bei, Li, Kuyper and Zhang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 This article was submitted to Plant Microbe Interactions, a section of the journal Frontiers in Microbiology Edited by: Choong-Min Ryu, Korea Research Institute of Bioscience and Biotechnology, South Korea Reviewed by: Weidong Kong, Institute of Tibetan Plateau Research (CAS), China; Aymé Spor, INRA UMR 1347 Agroécologie, France |
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SubjectTerms | high-throughput sequencing long-term phosphorus fertilization microbial ecological network Microbiology rhizocompartment soil microbiome |
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Title | Rhizoplane Bacteria and Plant Species Co-determine Phosphorus-Mediated Microbial Legacy Effect |
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