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Title: Organismal and spatial partitioning of energy and macronutrient transformations within a hypersaline mat

Abstract

Phototrophic mat communities are model ecosystems for studying energy cycling and elemental transformations because complete biogeochemical cycles occur over millimeter-to-centimeter scales. Characterization of energy and nutrient capture within hypersaline phototrophic mats has focused on specific processes and organisms, however little is known about community-wide distribution of and linkages between these processes. To investigate energy and macronutrient capture and flow through a structured community, the spatial and organismal distribution of metabolic functions within a compact hypersaline mat community from Hot Lake have been broadly elucidated through species-resolved metagenomics and geochemical, microbial diversity, and metabolic gradient measurements. Draft reconstructed genomes of abundant organisms revealed three dominant cyanobacterial populations differentially distributed across the top layers of the mat suggesting niche separation along light and oxygen gradients. Many organisms contained diverse functional profiles, allowing for metabolic response to changing conditions within the mat. Organisms with partial nitrogen and sulfur metabolisms were widespread indicating dependence upon metabolite exchange. In addition, changes in community spatial structure were observed over the diel. These results indicate that organisms within the mat community have adapted to the temporally dynamic environmental gradients in this hypersaline mat through metabolic flexibility and fluid syntrophic interactions, including shifts in spatial arrangements.

Authors:
; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1372983
Report Number(s):
PNNL-SA-124562
Journal ID: ISSN 1574-6941; 48418; KP1601010
DOE Contract Number:
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: FEMS Microbiology Ecology (Online); Journal Volume: 93; Journal Issue: 4
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; reconstructed genomes; metagenomics; hypersaline; magnesium sulfate; element; Environmental Molecular Sciences Laboratory

Citation Formats

Mobberley, Jennifer M., Lindemann, Stephen R., Bernstein, Hans C., Moran, James J., Renslow, Ryan S., Babauta, Jerome, Hu, Dehong, Beyenal, Haluk, and Nelson, William C. Organismal and spatial partitioning of energy and macronutrient transformations within a hypersaline mat. United States: N. p., 2017. Web. doi:10.1093/femsec/fix028.
Mobberley, Jennifer M., Lindemann, Stephen R., Bernstein, Hans C., Moran, James J., Renslow, Ryan S., Babauta, Jerome, Hu, Dehong, Beyenal, Haluk, & Nelson, William C. Organismal and spatial partitioning of energy and macronutrient transformations within a hypersaline mat. United States. doi:10.1093/femsec/fix028.
Mobberley, Jennifer M., Lindemann, Stephen R., Bernstein, Hans C., Moran, James J., Renslow, Ryan S., Babauta, Jerome, Hu, Dehong, Beyenal, Haluk, and Nelson, William C. Tue . "Organismal and spatial partitioning of energy and macronutrient transformations within a hypersaline mat". United States. doi:10.1093/femsec/fix028.
@article{osti_1372983,
title = {Organismal and spatial partitioning of energy and macronutrient transformations within a hypersaline mat},
author = {Mobberley, Jennifer M. and Lindemann, Stephen R. and Bernstein, Hans C. and Moran, James J. and Renslow, Ryan S. and Babauta, Jerome and Hu, Dehong and Beyenal, Haluk and Nelson, William C.},
abstractNote = {Phototrophic mat communities are model ecosystems for studying energy cycling and elemental transformations because complete biogeochemical cycles occur over millimeter-to-centimeter scales. Characterization of energy and nutrient capture within hypersaline phototrophic mats has focused on specific processes and organisms, however little is known about community-wide distribution of and linkages between these processes. To investigate energy and macronutrient capture and flow through a structured community, the spatial and organismal distribution of metabolic functions within a compact hypersaline mat community from Hot Lake have been broadly elucidated through species-resolved metagenomics and geochemical, microbial diversity, and metabolic gradient measurements. Draft reconstructed genomes of abundant organisms revealed three dominant cyanobacterial populations differentially distributed across the top layers of the mat suggesting niche separation along light and oxygen gradients. Many organisms contained diverse functional profiles, allowing for metabolic response to changing conditions within the mat. Organisms with partial nitrogen and sulfur metabolisms were widespread indicating dependence upon metabolite exchange. In addition, changes in community spatial structure were observed over the diel. These results indicate that organisms within the mat community have adapted to the temporally dynamic environmental gradients in this hypersaline mat through metabolic flexibility and fluid syntrophic interactions, including shifts in spatial arrangements.},
doi = {10.1093/femsec/fix028},
journal = {FEMS Microbiology Ecology (Online)},
number = 4,
volume = 93,
place = {United States},
year = {Tue Mar 21 00:00:00 EDT 2017},
month = {Tue Mar 21 00:00:00 EDT 2017}
}
  • To investigate the extent of genetic stratification in structured microbial communities, we compared the metagenomes of 10 successive layers of a phylogenetically complex hypersaline mat from Guerrero Negro, Mexico. We found pronounced millimeter-scale genetic gradients that are consistent with the physicochemical profile of the mat. Despite these gradients, all layers displayed near identical and acid-shifted isoelectric point profiles due to a molecular convergence of amino acid usage indicating that hypersalinity enforces an overriding selective pressure on the mat community.
  • Benthic microbial ecosystems are widespread yet knowledge gaps still remain on the relationships between the diversity of species across kingdoms and productivity. Here, we ask two fundamental questions: 1) How does species diversity relate to the rates of primary and heterotrophic productivity? 2) How do diel variations in light-energy inputs influence productivity and microbiome diversity? To answer these questions, microbial mats from a magnesium sulfate hypersaline Lake were used to establish microcosms. Both the number and relatedness between bacterial and eukaryotic taxa in the microbiome were assayed via amplicon based sequencing of 16S and 18S rRNA genes over two dielmore » cycles. These results correlated with biomass productivity obtained from substrate-specific 13C stable isotope incorporation that enabled comparisons between primary and heterotrophic productivity. Both bacterial and eukaryotic species richness and evenness were related only to the rates of 13C labeled glucose and acetate biomass incorporation. Interestingly, measures of these heterotrophic relationships changed from positive and negative correlations depending on carbon derived from glucose and acetate, respectively. Bacterial and eukaryotic diversity of this ecosystem is also controlled, in part, energy constraints imposed by changing irradiance over a diel cycle.« less
  • ABSTRACT The complete genome sequence ofCyanobacteriumsp. strain HL-69 consists of 3,155,247 bp and contains 2,897 predicted genes comprising a chromosome and two plasmids. The genome is consistent with a halophilic nondiazotrophic phototrophic lifestyle, and this organism is able to synthesize most B vitamins and produces several secondary metabolites.
  • Benthic microbial ecosystems are widespread yet knowledge gaps still remain on the relationships between the diversity of species across kingdoms and productivity. Here, we ask two fundamental questions: (i) How does species diversity relate to the rates of primary and heterotrophic productivity? (ii) How do diel variations in light-energy inputs influence productivity and microbiome diversity? To answer these questions, microbial mats from a magnesium sulfate hypersaline lake were used to establish microcosms. Both the number and relatedness between bacterial and eukaryotic taxa in the microbiome were assayed via amplicon-based sequencing of 16S and 18S rRNA genes over two diel cycles.more » These results correlated with biomass productivity obtained from substrate-specific 13C stable isotope tracers that enabled comparisons between primary and heterotrophic productivity. Both bacterial and eukaryotic species richness and evenness were related only to the rates of 13C-labeled glucose and acetate biomass incorporation. Interestingly, measures of these heterotrophic relationships changed from positive and negative correlations depending on carbon derived from glucose or acetate, respectively. The bacterial and eukaryotic diversity of this ecosystem is also controlled, in part, from energy constraints imposed by changing irradiance over a diel cycle.« less