skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Seasonal succession leads to habitat-dependent differentiation in ribosomal RNA:DNA ratios among freshwater lake bacteria

Abstract

Relative abundance profiles of bacterial populations measured by sequencing DNA or RNA of marker genes can widely differ. These differences, made apparent when calculating ribosomal RNA:DNA ratios, have been interpreted as variable activities of bacterial populations. However, inconsistent correlations between ribosomal RNA:DNA ratios and metabolic activity or growth rates have led to a more conservative interpretation of this metric as the cellular protein synthesis potential (PSP). Little is known, particularly in freshwater systems, about how PSP varies for specific taxa across temporal and spatial environmental gradients and how conserved PSP is across bacterial phylogeny. Here, we generated 16S rRNA gene sequencing data using simultaneously extracted DNA and RNA from fractionated (free-living and particulate) water samples taken seasonally along a eutrophic freshwater estuary to oligotrophic pelagic transect in Lake Michigan. In contrast to previous reports, we observed frequent clustering of DNA and RNA data from the same sample. Analysis of the overlap in taxa detected at the RNA and DNA level indicated that microbial dormancy may be more common in the estuary, the particulate fraction, and during the stratified period. Across spatiotemporal gradients, PSP was often conserved at the phylum and class levels. PSPs for specific taxa were more similar acrossmore » habitats in spring than in summer and fall. This was most notable for PSPs of the same taxa when located in the free-living or particulate fractions, but also when contrasting surface to deep, and estuary to Lake Michigan communities. Our results show that community composition assessed by RNA and DNA measurements are more similar than previously assumed in freshwater systems. Furthermore, the similarity between RNA and DNA measurements and taxa-specific PSPs that drive community-level similarities are conditional on spatiotemporal factors.« less

Authors:
 [1];  [1];  [1];  [1]
  1. Univ. of Michigan, Ann Arbor, MI (United States)
Publication Date:
Research Org.:
USDOE Office of Science (SC) (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1257632
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; estuary; great lakes; potential activity; protein synthesis potential; particle-associated; free-living; 16S rRNA

Citation Formats

Denef, Vincent J., Fujimoto, Masanori, Berry, Michelle A., and Schmidt, Marian L. Seasonal succession leads to habitat-dependent differentiation in ribosomal RNA:DNA ratios among freshwater lake bacteria. United States: N. p., 2016. Web. doi:10.3389/fmicb.2016.00606.
Denef, Vincent J., Fujimoto, Masanori, Berry, Michelle A., & Schmidt, Marian L. Seasonal succession leads to habitat-dependent differentiation in ribosomal RNA:DNA ratios among freshwater lake bacteria. United States. doi:10.3389/fmicb.2016.00606.
Denef, Vincent J., Fujimoto, Masanori, Berry, Michelle A., and Schmidt, Marian L. Fri . "Seasonal succession leads to habitat-dependent differentiation in ribosomal RNA:DNA ratios among freshwater lake bacteria". United States. doi:10.3389/fmicb.2016.00606. https://www.osti.gov/servlets/purl/1257632.
@article{osti_1257632,
title = {Seasonal succession leads to habitat-dependent differentiation in ribosomal RNA:DNA ratios among freshwater lake bacteria},
author = {Denef, Vincent J. and Fujimoto, Masanori and Berry, Michelle A. and Schmidt, Marian L.},
abstractNote = {Relative abundance profiles of bacterial populations measured by sequencing DNA or RNA of marker genes can widely differ. These differences, made apparent when calculating ribosomal RNA:DNA ratios, have been interpreted as variable activities of bacterial populations. However, inconsistent correlations between ribosomal RNA:DNA ratios and metabolic activity or growth rates have led to a more conservative interpretation of this metric as the cellular protein synthesis potential (PSP). Little is known, particularly in freshwater systems, about how PSP varies for specific taxa across temporal and spatial environmental gradients and how conserved PSP is across bacterial phylogeny. Here, we generated 16S rRNA gene sequencing data using simultaneously extracted DNA and RNA from fractionated (free-living and particulate) water samples taken seasonally along a eutrophic freshwater estuary to oligotrophic pelagic transect in Lake Michigan. In contrast to previous reports, we observed frequent clustering of DNA and RNA data from the same sample. Analysis of the overlap in taxa detected at the RNA and DNA level indicated that microbial dormancy may be more common in the estuary, the particulate fraction, and during the stratified period. Across spatiotemporal gradients, PSP was often conserved at the phylum and class levels. PSPs for specific taxa were more similar across habitats in spring than in summer and fall. This was most notable for PSPs of the same taxa when located in the free-living or particulate fractions, but also when contrasting surface to deep, and estuary to Lake Michigan communities. Our results show that community composition assessed by RNA and DNA measurements are more similar than previously assumed in freshwater systems. Furthermore, the similarity between RNA and DNA measurements and taxa-specific PSPs that drive community-level similarities are conditional on spatiotemporal factors.},
doi = {10.3389/fmicb.2016.00606},
journal = {Frontiers in Microbiology},
number = ,
volume = 7,
place = {United States},
year = {2016},
month = {4}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Save / Share:

Works referenced in this record:

Metacommunity dynamics of bacteria in an arctic lake: the impact of species sorting and mass effects on bacterial production and biogeography
journal, March 2014


The Ecological Role of Water-Column Microbes in the Sea
journal, January 1983

  • Azam, F.; Fenchel, T.; Field, Jg
  • Marine Ecology Progress Series, Vol. 10
  • DOI: 10.3354/meps010257

Active and total microbial communities in forest soil are largely different and highly stratified during decomposition
journal, July 2011

  • Baldrian, Petr; Kolařík, Miroslav; Štursová, Martina
  • The ISME Journal, Vol. 6, Issue 2
  • DOI: 10.1038/ismej.2011.95

Responses of soil bacterial and fungal communities to extreme desiccation and rewetting
journal, July 2013

  • Barnard, Romain L.; Osborne, Catherine A.; Firestone, Mary K.
  • The ISME Journal, Vol. 7, Issue 11
  • DOI: 10.1038/ismej.2013.104

Comparison of bacterial communities on limnic versus coastal marine particles reveals profound differences in colonization: Marine and limnic particle-associated bacteria
journal, April 2014

  • Bižić-Ionescu, Mina; Zeder, Michael; Ionescu, Danny
  • Environmental Microbiology, Vol. 17, Issue 10
  • DOI: 10.1111/1462-2920.12466

Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses
journal, July 2013

  • Blazewicz, Steven J.; Barnard, Romain L.; Daly, Rebecca A.
  • The ISME Journal, Vol. 7, Issue 11
  • DOI: 10.1038/ismej.2013.102

Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient
journal, August 2012


Activity of abundant and rare bacteria in a coastal ocean
journal, July 2011

  • Campbell, B. J.; Yu, L.; Heidelberg, J. F.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 31
  • DOI: 10.1073/pnas.1101405108

Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012

  • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.8

Chloroflexi CL500-11 Populations That Predominate Deep-Lake Hypolimnion Bacterioplankton Rely on Nitrogen-Rich Dissolved Organic Matter Metabolism and C 1 Compound Oxidation
journal, December 2015

  • Denef, Vincent J.; Mueller, Ryan S.; Chiang, Edna
  • Applied and Environmental Microbiology, Vol. 82, Issue 5
  • DOI: 10.1128/AEM.03014-15

Microbial community structure and function on sinking particles in the North Pacific Subtropical Gyre
journal, May 2015


Community composition and activity state of estuarine bacterioplankton assessed using differential staining and metagenomic analysis of 16S rDNA and rRNA
journal, July 2013

  • Franklin, Rb; Luria, C.; Shozo Ozaki, L.
  • Aquatic Microbial Ecology, Vol. 69, Issue 3
  • DOI: 10.3354/ame01635

Relationship between phytoplankton cell size and the rate of orthophosphate uptake: in situ observations of an estuarine population
journal, January 1978

  • Friebele, E. S.; Correll, D. L.; Faust, M. A.
  • Marine Biology, Vol. 45, Issue 1
  • DOI: 10.1007/BF00388976

Intracellular Compartmentation in Planctomycetes
journal, October 2005


Major contribution of both zooplankton and protists to the top-down regulation of freshwater aerobic anoxygenic phototrophic bacteria
journal, September 2015

  • Garcia-Chaves, Mc; Cottrell, Mt; Kirchman, Dl
  • Aquatic Microbial Ecology, Vol. 76, Issue 1
  • DOI: 10.3354/ame01770

Study of bacterial communities in Antarctic coastal waters by a combination of 16S rRNA and 16S rDNA sequencing
journal, December 2006


Diversity of total and active free-living vs. particle-attached bacteria in the euphotic zone of the NW Mediterranean Sea
journal, October 2009


Comparison of cell-specific activity between free-living and attached bacteria using isolates and natural assemblages
journal, January 2007


Isolation of Novel Ultramicrobacteria Classified as Actinobacteria from Five Freshwater Habitats in Europe and Asia
journal, March 2003


Relationship between Abundance and Specific Activity of Bacterioplankton in Open Ocean Surface Waters
journal, October 2012

  • Hunt, Dana E.; Lin, Yajuan; Church, Matthew J.
  • Applied and Environmental Microbiology, Vol. 79, Issue 1
  • DOI: 10.1128/AEM.02155-12

Vertical Distribution of Functional Potential and Active Microbial Communities in Meromictic Lake Kivu
journal, April 2015


Dormancy contributes to the maintenance of microbial diversity
journal, March 2010

  • Jones, S. E.; Lennon, J. T.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 13
  • DOI: 10.1073/pnas.0912765107

Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform
journal, June 2013

  • Kozich, James J.; Westcott, Sarah L.; Baxter, Nielson T.
  • Applied and Environmental Microbiology, Vol. 79, Issue 17
  • DOI: 10.1128/AEM.01043-13

Annual patterns of presence and activity of marine bacteria monitored by 16S rDNA–16S rRNA fingerprints in the coastal NW Mediterranean Sea
journal, February 2009

  • Lami, R.; Ghiglione, Jf; Desdevises, Y.
  • Aquatic Microbial Ecology, Vol. 54
  • DOI: 10.3354/ame01264

Growth rates and rRNA content of four marine bacteria in pure cultures and in the Delaware estuary
journal, September 2015

  • Lankiewicz, Thomas S.; Cottrell, Matthew T.; Kirchman, David L.
  • The ISME Journal, Vol. 10, Issue 4
  • DOI: 10.1038/ismej.2015.156

Microbial seed banks: the ecological and evolutionary implications of dormancy
journal, January 2011

  • Lennon, Jay T.; Jones, Stuart E.
  • Nature Reviews Microbiology, Vol. 9, Issue 2
  • DOI: 10.1038/nrmicro2504

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014


Acidobacteria dominate the active bacterial communities of Arctic tundra with widely divergent winter-time snow accumulation and soil temperatures
journal, November 2012

  • Männistö, Minna K.; Kurhela, Emilia; Tiirola, Marja
  • FEMS Microbiology Ecology, Vol. 84, Issue 1
  • DOI: 10.1111/1574-6941.12035

Phylogenetic conservatism of functional traits in microorganisms
journal, December 2012

  • Martiny, Adam C.; Treseder, Kathleen; Pusch, Gordon
  • The ISME Journal, Vol. 7, Issue 4
  • DOI: 10.1038/ismej.2012.160

RNA Preservation Agents and Nucleic Acid Extraction Method Bias Perceived Bacterial Community Composition
journal, March 2015


phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013


Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible
journal, April 2014


Metagenomic Sequencing of an In Vitro-Simulated Microbial Community
journal, April 2010


A single-cell view on the ecophysiology of anaerobic phototrophic bacteria
journal, November 2008

  • Musat, N.; Halm, H.; Winterholler, B.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 46
  • DOI: 10.1073/pnas.0809329105

A Guide to the Natural History of Freshwater Lake Bacteria
journal, March 2011

  • Newton, R. J.; Jones, S. E.; Eiler, A.
  • Microbiology and Molecular Biology Reviews, Vol. 75, Issue 1
  • DOI: 10.1128/MMBR.00028-10

The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

Long-Term Characterization of Free-Living and Particle-Associated Bacterial Communities in Lake Tiefwaren Reveals Distinct Seasonal Patterns
journal, April 2012


Particle-association lifestyle is a phylogenetically conserved trait in bathypelagic prokaryotes
journal, November 2015

  • Salazar, Guillem; Cornejo-Castillo, Francisco M.; Borrull, Encarna
  • Molecular Ecology, Vol. 24, Issue 22
  • DOI: 10.1111/mec.13419

The ecology of pelagic freshwater methylotrophs assessed by a high-resolution monitoring and isolation campaign
journal, May 2015

  • Salcher, Michaela M.; Neuenschwander, Stefan M.; Posch, Thomas
  • The ISME Journal, Vol. 9, Issue 11
  • DOI: 10.1038/ismej.2015.55

Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria ‘that rule the waves’ (LD12)
journal, March 2011

  • Salcher, Michaela M.; Pernthaler, Jakob; Posch, Thomas
  • The ISME Journal, Vol. 5, Issue 8
  • DOI: 10.1038/ismej.2011.8

In situ substrate preferences of abundant bacterioplankton populations in a prealpine freshwater lake
journal, December 2012

  • Salcher, Michaela M.; Posch, Thomas; Pernthaler, Jakob
  • The ISME Journal, Vol. 7, Issue 5
  • DOI: 10.1038/ismej.2012.162

Reducing the Effects of PCR Amplification and Sequencing Artifacts on 16S rRNA-Based Studies
journal, December 2011


Phylogenetic conservation of freshwater lake habitat preference varies between abundant bacterioplankton phyla: Bacterial habitat preferences in freshwater lakes
journal, January 2016

  • Schmidt, Marian L.; White, Jeffrey D.; Denef, Vincent J.
  • Environmental Microbiology, Vol. 18, Issue 4
  • DOI: 10.1111/1462-2920.13143

Leucine incorporation by aerobic anoxygenic phototrophic bacteria in the Delaware estuary
journal, May 2014

  • Stegman, Monica R.; Cottrell, Matthew T.; Kirchman, David L.
  • The ISME Journal, Vol. 8, Issue 11
  • DOI: 10.1038/ismej.2014.75

Current Status and Trends in Muskegon Lake, Michigan
journal, March 2008


Different bulk and active bacterial communities in cryoconite from the margin and interior of the Greenland ice sheet: Bulk and active bacteria in Greenland cryoconite
journal, January 2015

  • Stibal, Marek; Schostag, Morten; Cameron, Karen A.
  • Environmental Microbiology Reports, Vol. 7, Issue 2
  • DOI: 10.1111/1758-2229.12246

Evaluation of metatranscriptomic protocols and application to the study of freshwater microbial communities: Metatranscriptomics of freshwater communities
journal, June 2014

  • Tsementzi, Despina; Poretsky, Rachel; Rodriguez-R, Luis M.
  • Environmental Microbiology Reports, Vol. 6, Issue 6
  • DOI: 10.1111/1758-2229.12180

Dreissena and the disappearance of the spring phytoplankton bloom in Lake Michigan
journal, January 2010

  • Vanderploeg, Henry A.; Liebig, James R.; Nalepa, Thomas F.
  • Journal of Great Lakes Research, Vol. 36
  • DOI: 10.1016/j.jglr.2010.04.005

Drivers shaping the diversity and biogeography of total and active bacterial communities in the South China Sea
journal, April 2014

  • Zhang, Yao; Zhao, Zihao; Dai, Minhan
  • Molecular Ecology, Vol. 23, Issue 9
  • DOI: 10.1111/mec.12739

Reproducibility and quantitation of amplicon sequencing-based detection
journal, February 2011


    Works referencing / citing this record:

    Microbial Mat Compositional and Functional Sensitivity to Environmental Disturbance
    journal, October 2016


    Microbial Mat Compositional and Functional Sensitivity to Environmental Disturbance
    journal, October 2016