Examining the Effects of the Nitrogen Environment on Growth and N(2)-Fixation of Endophytic Herbaspirillum seropedicae in Maize Seedlings by Applying (11)C Radiotracing

Herbaspirillum seropedicae, as an endophyte and prolific root colonizer of numerous cereal crops, occupies an important ecological niche in agriculture because of its ability to promote plant growth and potentially improve crop yield. More importantly, there exists the untapped potential to harness...

Descripción completa

Detalles Bibliográficos
Autores principales: Waller, Spenser, Wilder, Stacy L., Schueller, Michael J., Housh, Alexandra B., Scott, Stephanie, Benoit, Mary, Powell, Avery, Powell, Garren, Ferrieri, Richard A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8401641/
https://www.ncbi.nlm.nih.gov/pubmed/34442661
http://dx.doi.org/10.3390/microorganisms9081582
_version_ 1783745599252725760
author Waller, Spenser
Wilder, Stacy L.
Schueller, Michael J.
Housh, Alexandra B.
Scott, Stephanie
Benoit, Mary
Powell, Avery
Powell, Garren
Ferrieri, Richard A.
author_facet Waller, Spenser
Wilder, Stacy L.
Schueller, Michael J.
Housh, Alexandra B.
Scott, Stephanie
Benoit, Mary
Powell, Avery
Powell, Garren
Ferrieri, Richard A.
author_sort Waller, Spenser
collection PubMed
description Herbaspirillum seropedicae, as an endophyte and prolific root colonizer of numerous cereal crops, occupies an important ecological niche in agriculture because of its ability to promote plant growth and potentially improve crop yield. More importantly, there exists the untapped potential to harness its ability, as a diazotroph, to fix atmospheric N(2) as an alternative nitrogen resource to synthetic fertilizers. While mechanisms for plant growth promotion remain controversial, especially in cereal crops, one irrefutable fact is these microorganisms rely heavily on plant-borne carbon as their main energy source in support of their own growth and biological functions. Biological nitrogen fixation (BNF), a microbial function that is reliant on nitrogenase enzyme activity, is extremely sensitive to the localized nitrogen environment of the microorganism. However, whether internal root colonization can serve to shield the microorganisms and de-sensitize nitrogenase activity to changes in the soil nitrogen status remains unanswered. We used RAM10, a GFP-reporting strain of H. seropedicae, and administered radioactive (11)CO(2) tracer to intact 3-week-old maize leaves and followed (11)C-photosynthates to sites within intact roots where actively fluorescing microbial colonies assimilated the tracer. We examined the influence of administering either 1 mM or 10 mM nitrate during plant growth on microbial demands for plant-borne (11)C. Nitrogenase activity was also examined under the same growth conditions using the acetylene reduction assay. We found that plant growth under low nitrate resulted in higher nitrogenase activity as well as higher microbial demands for plant-borne carbon than plant growth under high nitrate. However, carbon availability was significantly diminished under low nitrate growth due to reduced host CO(2) fixation and reduced allocation of carbon resources to the roots. This response of the host caused significant inhibition of microbial growth. In summary, internal root colonization did little to shield these endophytic microorganisms from the nitrogen environment.
format Online
Article
Text
id pubmed-8401641
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-84016412021-08-29 Examining the Effects of the Nitrogen Environment on Growth and N(2)-Fixation of Endophytic Herbaspirillum seropedicae in Maize Seedlings by Applying (11)C Radiotracing Waller, Spenser Wilder, Stacy L. Schueller, Michael J. Housh, Alexandra B. Scott, Stephanie Benoit, Mary Powell, Avery Powell, Garren Ferrieri, Richard A. Microorganisms Article Herbaspirillum seropedicae, as an endophyte and prolific root colonizer of numerous cereal crops, occupies an important ecological niche in agriculture because of its ability to promote plant growth and potentially improve crop yield. More importantly, there exists the untapped potential to harness its ability, as a diazotroph, to fix atmospheric N(2) as an alternative nitrogen resource to synthetic fertilizers. While mechanisms for plant growth promotion remain controversial, especially in cereal crops, one irrefutable fact is these microorganisms rely heavily on plant-borne carbon as their main energy source in support of their own growth and biological functions. Biological nitrogen fixation (BNF), a microbial function that is reliant on nitrogenase enzyme activity, is extremely sensitive to the localized nitrogen environment of the microorganism. However, whether internal root colonization can serve to shield the microorganisms and de-sensitize nitrogenase activity to changes in the soil nitrogen status remains unanswered. We used RAM10, a GFP-reporting strain of H. seropedicae, and administered radioactive (11)CO(2) tracer to intact 3-week-old maize leaves and followed (11)C-photosynthates to sites within intact roots where actively fluorescing microbial colonies assimilated the tracer. We examined the influence of administering either 1 mM or 10 mM nitrate during plant growth on microbial demands for plant-borne (11)C. Nitrogenase activity was also examined under the same growth conditions using the acetylene reduction assay. We found that plant growth under low nitrate resulted in higher nitrogenase activity as well as higher microbial demands for plant-borne carbon than plant growth under high nitrate. However, carbon availability was significantly diminished under low nitrate growth due to reduced host CO(2) fixation and reduced allocation of carbon resources to the roots. This response of the host caused significant inhibition of microbial growth. In summary, internal root colonization did little to shield these endophytic microorganisms from the nitrogen environment. MDPI 2021-07-25 /pmc/articles/PMC8401641/ /pubmed/34442661 http://dx.doi.org/10.3390/microorganisms9081582 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Waller, Spenser
Wilder, Stacy L.
Schueller, Michael J.
Housh, Alexandra B.
Scott, Stephanie
Benoit, Mary
Powell, Avery
Powell, Garren
Ferrieri, Richard A.
Examining the Effects of the Nitrogen Environment on Growth and N(2)-Fixation of Endophytic Herbaspirillum seropedicae in Maize Seedlings by Applying (11)C Radiotracing
title Examining the Effects of the Nitrogen Environment on Growth and N(2)-Fixation of Endophytic Herbaspirillum seropedicae in Maize Seedlings by Applying (11)C Radiotracing
title_full Examining the Effects of the Nitrogen Environment on Growth and N(2)-Fixation of Endophytic Herbaspirillum seropedicae in Maize Seedlings by Applying (11)C Radiotracing
title_fullStr Examining the Effects of the Nitrogen Environment on Growth and N(2)-Fixation of Endophytic Herbaspirillum seropedicae in Maize Seedlings by Applying (11)C Radiotracing
title_full_unstemmed Examining the Effects of the Nitrogen Environment on Growth and N(2)-Fixation of Endophytic Herbaspirillum seropedicae in Maize Seedlings by Applying (11)C Radiotracing
title_short Examining the Effects of the Nitrogen Environment on Growth and N(2)-Fixation of Endophytic Herbaspirillum seropedicae in Maize Seedlings by Applying (11)C Radiotracing
title_sort examining the effects of the nitrogen environment on growth and n(2)-fixation of endophytic herbaspirillum seropedicae in maize seedlings by applying (11)c radiotracing
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8401641/
https://www.ncbi.nlm.nih.gov/pubmed/34442661
http://dx.doi.org/10.3390/microorganisms9081582
work_keys_str_mv AT wallerspenser examiningtheeffectsofthenitrogenenvironmentongrowthandn2fixationofendophyticherbaspirillumseropedicaeinmaizeseedlingsbyapplying11cradiotracing
AT wilderstacyl examiningtheeffectsofthenitrogenenvironmentongrowthandn2fixationofendophyticherbaspirillumseropedicaeinmaizeseedlingsbyapplying11cradiotracing
AT schuellermichaelj examiningtheeffectsofthenitrogenenvironmentongrowthandn2fixationofendophyticherbaspirillumseropedicaeinmaizeseedlingsbyapplying11cradiotracing
AT houshalexandrab examiningtheeffectsofthenitrogenenvironmentongrowthandn2fixationofendophyticherbaspirillumseropedicaeinmaizeseedlingsbyapplying11cradiotracing
AT scottstephanie examiningtheeffectsofthenitrogenenvironmentongrowthandn2fixationofendophyticherbaspirillumseropedicaeinmaizeseedlingsbyapplying11cradiotracing
AT benoitmary examiningtheeffectsofthenitrogenenvironmentongrowthandn2fixationofendophyticherbaspirillumseropedicaeinmaizeseedlingsbyapplying11cradiotracing
AT powellavery examiningtheeffectsofthenitrogenenvironmentongrowthandn2fixationofendophyticherbaspirillumseropedicaeinmaizeseedlingsbyapplying11cradiotracing
AT powellgarren examiningtheeffectsofthenitrogenenvironmentongrowthandn2fixationofendophyticherbaspirillumseropedicaeinmaizeseedlingsbyapplying11cradiotracing
AT ferrieriricharda examiningtheeffectsofthenitrogenenvironmentongrowthandn2fixationofendophyticherbaspirillumseropedicaeinmaizeseedlingsbyapplying11cradiotracing