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

Abstract

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.

Authors:
 [1];  [2];  [2];  [3];  [2];  [2];  [2];  [4];  [4];  [2];  [2];  [2]
  1. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division; Purdue Univ., West Lafayette, IN (United States). Whistler Center for Carbohydrate Research and Department of Nutrition Science
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division
  3. Purdue Univ., West Lafayette, IN (United States). Whistler Center for Carbohydrate Research
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1415085
Report Number(s):
PNNL-SA-129376
Journal ID: ISSN 1664-302X; KP1601010
Grant/Contract Number:  
AC05-76RL01830; AC02-05CH11231
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; carbon fixation; nitrate reduction; phosphate transport; sulfate reduction; metagenomics; metatranscriptomics; metaproteomics; periphyton

Citation Formats

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., and Romine, Margaret F. Predicting Species-Resolved Macronutrient Acquisition during Succession in a Model Phototrophic Biofilm Using an Integrated ‘Omics Approach. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.01020.
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. United States. doi:10.3389/fmicb.2017.01020.
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., and Romine, Margaret F. Tue . "Predicting Species-Resolved Macronutrient Acquisition during Succession in a Model Phototrophic Biofilm Using an Integrated ‘Omics Approach". United States. doi:10.3389/fmicb.2017.01020. https://www.osti.gov/servlets/purl/1415085.
@article{osti_1415085,
title = {Predicting Species-Resolved Macronutrient Acquisition during Succession in a Model Phototrophic Biofilm Using an Integrated ‘Omics Approach},
author = {Lindemann, Stephen R. and Mobberley, Jennifer M. and Cole, Jessica K. and Markillie, L. M. and Taylor, Ronald C. and Huang, Eric and Chrisler, William B. and Wiley, H. S. and Lipton, Mary S. and Nelson, William C. and Fredrickson, James K. and Romine, Margaret F.},
abstractNote = {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.},
doi = {10.3389/fmicb.2017.01020},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {Tue Jun 13 00:00:00 EDT 2017},
month = {Tue Jun 13 00:00:00 EDT 2017}
}

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