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Predicting Species-Resolved Macronutrient Acquisition during Succession in a Model Phototrophic Biofilm Using an Integrated ‘Omics Approach

The principles governing acquisition and interspecies exchange of nutrients in microbial communities and how those exchanges impact community productivity are poorly understood. Here, we examine energy and macronutrient acquisition in unicyanobacterial consortia for which species-resolved genome inf...

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Autores principales: Lindemann, Stephen R., Mobberley, Jennifer M., Cole, Jessica K., Markillie, L. M., Taylor, Ronald C., Huang, Eric, Chrisler, William B., Wiley, H. S., Lipton, Mary S., Nelson, William C., Fredrickson, James K., Romine, Margaret F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5468372/
https://www.ncbi.nlm.nih.gov/pubmed/28659875
http://dx.doi.org/10.3389/fmicb.2017.01020
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author Lindemann, Stephen R.
Mobberley, Jennifer M.
Cole, Jessica K.
Markillie, L. M.
Taylor, Ronald C.
Huang, Eric
Chrisler, William B.
Wiley, H. S.
Lipton, Mary S.
Nelson, William C.
Fredrickson, James K.
Romine, Margaret F.
author_facet Lindemann, Stephen R.
Mobberley, Jennifer M.
Cole, Jessica K.
Markillie, L. M.
Taylor, Ronald C.
Huang, Eric
Chrisler, William B.
Wiley, H. S.
Lipton, Mary S.
Nelson, William C.
Fredrickson, James K.
Romine, Margaret F.
author_sort Lindemann, Stephen R.
collection PubMed
description The principles governing acquisition and interspecies exchange of nutrients in microbial communities and how those exchanges impact community productivity are poorly understood. Here, we examine energy and macronutrient acquisition in unicyanobacterial consortia for which species-resolved genome information exists for all members, allowing us to use multi-omic approaches to predict species’ abilities to acquire resources and examine expression of resource-acquisition genes during succession. Metabolic reconstruction indicated that a majority of heterotrophic community members lacked the genes required to directly acquire the inorganic nutrients provided in culture medium, suggesting high metabolic interdependency. The sole primary producer in consortium UCC-O, cyanobacterium Phormidium sp. OSCR, displayed declining expression of energy harvest, carbon fixation, and nitrate and sulfate reduction proteins but sharply increasing phosphate transporter expression over 28 days. Most heterotrophic members likewise exhibited signs of phosphorus starvation during succession. Though similar in their responses to phosphorus limitation, heterotrophs displayed species-specific expression of nitrogen acquisition genes. These results suggest niche partitioning around nitrogen sources may structure the community when organisms directly compete for limited phosphate. Such niche complementarity around nitrogen sources may increase community diversity and productivity in phosphate-limited phototrophic communities.
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spelling pubmed-54683722017-06-28 Predicting Species-Resolved Macronutrient Acquisition during Succession in a Model Phototrophic Biofilm Using an Integrated ‘Omics Approach Lindemann, Stephen R. Mobberley, Jennifer M. Cole, Jessica K. Markillie, L. M. Taylor, Ronald C. Huang, Eric Chrisler, William B. Wiley, H. S. Lipton, Mary S. Nelson, William C. Fredrickson, James K. Romine, Margaret F. Front Microbiol Microbiology The principles governing acquisition and interspecies exchange of nutrients in microbial communities and how those exchanges impact community productivity are poorly understood. Here, we examine energy and macronutrient acquisition in unicyanobacterial consortia for which species-resolved genome information exists for all members, allowing us to use multi-omic approaches to predict species’ abilities to acquire resources and examine expression of resource-acquisition genes during succession. Metabolic reconstruction indicated that a majority of heterotrophic community members lacked the genes required to directly acquire the inorganic nutrients provided in culture medium, suggesting high metabolic interdependency. The sole primary producer in consortium UCC-O, cyanobacterium Phormidium sp. OSCR, displayed declining expression of energy harvest, carbon fixation, and nitrate and sulfate reduction proteins but sharply increasing phosphate transporter expression over 28 days. Most heterotrophic members likewise exhibited signs of phosphorus starvation during succession. Though similar in their responses to phosphorus limitation, heterotrophs displayed species-specific expression of nitrogen acquisition genes. These results suggest niche partitioning around nitrogen sources may structure the community when organisms directly compete for limited phosphate. Such niche complementarity around nitrogen sources may increase community diversity and productivity in phosphate-limited phototrophic communities. Frontiers Media S.A. 2017-06-13 /pmc/articles/PMC5468372/ /pubmed/28659875 http://dx.doi.org/10.3389/fmicb.2017.01020 Text en Copyright © 2017 Lindemann, Mobberley, Cole, Markillie, Taylor, Huang, Chrisler, Wiley, Lipton, Nelson, Fredrickson and Romine. http://creativecommons.org/licenses/by/4.0/ 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) or licensor 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.
spellingShingle Microbiology
Lindemann, Stephen R.
Mobberley, Jennifer M.
Cole, Jessica K.
Markillie, L. M.
Taylor, Ronald C.
Huang, Eric
Chrisler, William B.
Wiley, H. S.
Lipton, Mary S.
Nelson, William C.
Fredrickson, James K.
Romine, Margaret F.
Predicting Species-Resolved Macronutrient Acquisition during Succession in a Model Phototrophic Biofilm Using an Integrated ‘Omics Approach
title Predicting Species-Resolved Macronutrient Acquisition during Succession in a Model Phototrophic Biofilm Using an Integrated ‘Omics Approach
title_full Predicting Species-Resolved Macronutrient Acquisition during Succession in a Model Phototrophic Biofilm Using an Integrated ‘Omics Approach
title_fullStr Predicting Species-Resolved Macronutrient Acquisition during Succession in a Model Phototrophic Biofilm Using an Integrated ‘Omics Approach
title_full_unstemmed Predicting Species-Resolved Macronutrient Acquisition during Succession in a Model Phototrophic Biofilm Using an Integrated ‘Omics Approach
title_short Predicting Species-Resolved Macronutrient Acquisition during Succession in a Model Phototrophic Biofilm Using an Integrated ‘Omics Approach
title_sort predicting species-resolved macronutrient acquisition during succession in a model phototrophic biofilm using an integrated ‘omics approach
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5468372/
https://www.ncbi.nlm.nih.gov/pubmed/28659875
http://dx.doi.org/10.3389/fmicb.2017.01020
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