Primary and heterotrophic productivity relate to multikingdom diversity in a hypersaline mat
Abstract
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. 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.
- Authors:
-
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division; Washington State Univ., Pullman, WA (United States). The Gene and Linda Voiland School of Chemical Engineering and Bioengineering
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Signature Science and Technology Division
- 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)
- OSTI Identifier:
- 1413512
- Report Number(s):
- PNNL-SA-127139
Journal ID: ISSN 1574-6941
- Grant/Contract Number:
- AC05-76RL01830
- Resource Type:
- Accepted Manuscript
- Journal Name:
- FEMS Microbiology Ecology (Online)
- Additional Journal Information:
- Journal Name: FEMS Microbiology Ecology (Online); Journal Volume: 93; Journal Issue: 10; Journal ID: ISSN 1574-6941
- Publisher:
- Federation of European Microbiological Societies
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; diversity; productivity; microbial mat; stable isotope; hypersaline
Citation Formats
Bernstein, Hans C., Brislawn, Colin J., Dana, Karl, Flores-Wentz, Tobias, Cory, Alexandra B., Fansler, Sarah J., Fredrickson, James K., and Moran, James J.. Primary and heterotrophic productivity relate to multikingdom diversity in a hypersaline mat. United States: N. p., 2017.
Web. doi:10.1093/FEMSEC/FIX121.
Bernstein, Hans C., Brislawn, Colin J., Dana, Karl, Flores-Wentz, Tobias, Cory, Alexandra B., Fansler, Sarah J., Fredrickson, James K., & Moran, James J.. Primary and heterotrophic productivity relate to multikingdom diversity in a hypersaline mat. United States. https://doi.org/10.1093/FEMSEC/FIX121
Bernstein, Hans C., Brislawn, Colin J., Dana, Karl, Flores-Wentz, Tobias, Cory, Alexandra B., Fansler, Sarah J., Fredrickson, James K., and Moran, James J.. Tue .
"Primary and heterotrophic productivity relate to multikingdom diversity in a hypersaline mat". United States. https://doi.org/10.1093/FEMSEC/FIX121. https://www.osti.gov/servlets/purl/1413512.
@article{osti_1413512,
title = {Primary and heterotrophic productivity relate to multikingdom diversity in a hypersaline mat},
author = {Bernstein, Hans C. and Brislawn, Colin J. and Dana, Karl and Flores-Wentz, Tobias and Cory, Alexandra B. and Fansler, Sarah J. and Fredrickson, James K. and Moran, James J.},
abstractNote = {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. 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.},
doi = {10.1093/FEMSEC/FIX121},
journal = {FEMS Microbiology Ecology (Online)},
number = 10,
volume = 93,
place = {United States},
year = {2017},
month = {10}
}
Web of Science
Works referenced in this record:
Role of microbial mats in Sulaibikhat Bay (Kuwait) mudflat food webs: evidence from δ13C analysis
journal, February 2006
- Al-Zaidan, Asy; Kennedy, H.; Jones, Da
- Marine Ecology Progress Series, Vol. 308
Bacterial, archaeal and eukaryotic diversity of smooth and pustular microbial mat communities in the hypersaline lagoon of Shark Bay
journal, January 2009
- Allen, M. A.; Goh, F.; Burns, B. P.
- Geobiology, Vol. 7, Issue 1
A Method for Studying Protistan Diversity Using Massively Parallel Sequencing of V9 Hypervariable Regions of Small-Subunit Ribosomal RNA Genes
journal, July 2009
- Amaral-Zettler, Linda A.; McCliment, Elizabeth A.; Ducklow, Hugh W.
- PLoS ONE, Vol. 4, Issue 7
Some Limnological Features of a Shallow Saline Meromictic Lake
journal, July 1958
- Anderson, G. C.
- Limnology and Oceanography, Vol. 3, Issue 3
Biodiversity of the Hypersaline Urmia Lake National Park (NW Iran)
journal, February 2014
- Asem, Alireza; Eimanifar, Amin; Djamali, Morteza
- Diversity, Vol. 6, Issue 1
Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies
journal, July 1996
- Canfield, Donald E.; Teske, Andreas
- Nature, Vol. 382, Issue 6587
QIIME allows analysis of high-throughput community sequencing data
journal, April 2010
- Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
- Nature Methods, Vol. 7, Issue 5
Locally Weighted Regression: An Approach to Regression Analysis by Local Fitting
journal, September 1988
- Cleveland, William S.; Devlin, Susan J.
- Journal of the American Statistical Association, Vol. 83, Issue 403
Phototrophic biofilm assembly in microbial-mat-derived unicyanobacterial consortia: model systems for the study of autotroph-heterotroph interactions
journal, April 2014
- Cole, Jessica K.; Hutchison, Janine R.; Renslow, Ryan S.
- Frontiers in Microbiology, Vol. 5
New Guidelines for δ 13 C Measurements
journal, April 2006
- Coplen, Tyler B.; Brand, Willi A.; Gehre, Matthias
- Analytical Chemistry, Vol. 78, Issue 7
Search and clustering orders of magnitude faster than BLAST
journal, August 2010
- Edgar, Robert C.
- Bioinformatics, Vol. 26, Issue 19, p. 2460-2461
UCHIME improves sensitivity and speed of chimera detection
journal, June 2011
- Edgar, Robert C.; Haas, Brian J.; Clemente, Jose C.
- Bioinformatics, Vol. 27, Issue 16
Benthic primary production and O 2 -CO 2 dynamics in a shallow-water sediment: Spatial and temporal heterogeneity
journal, November 2000
- Fenchel, Tom; Glud, Ronnie N.
- Ophelia, Vol. 53, Issue 2
Meeting Report: The Terabase Metagenomics Workshop and the Vision of an Earth Microbiome Project
journal, January 2010
- Gilbert, Jack A.; Meyer, Folker; Antonopoulos, Dion
- Standards in Genomic Sciences, Vol. 3, Issue 3
Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data
journal, August 2009
- Hamady, Micah; Lozupone, Catherine; Knight, Rob
- The ISME Journal, Vol. 4, Issue 1
When should species richness be energy limited, and how would we know?
journal, January 2014
- Hurlbert, Allen H.; Stegen, James C.
- Ecology Letters, Vol. 17, Issue 4
Unexpected Diversity and Complexity of the Guerrero Negro Hypersaline Microbial Mat
journal, May 2006
- Ley, R. E.; Harris, J. K.; Wilcox, J.
- Applied and Environmental Microbiology, Vol. 72, Issue 5
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea
journal, December 2011
- McDonald, Daniel; Price, Morgan N.; Goodrich, Julia
- The ISME Journal, Vol. 6, Issue 3
Microphytobenthos: The Ecological Role of the "Secret Garden" of Unvegetated, Shallow-Water Marine Habitats. I. Distribution, Abundance and Primary Production
journal, June 1996
- MacIntyre, Hugh L.; Geider, Richard J.; Miller, Douglas C.
- Estuaries, Vol. 19, Issue 2
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013
- McMurdie, Paul J.; Holmes, Susan
- PLoS ONE, Vol. 8, Issue 4
Microphytobenthos: The Ecological Role of the "Secret Garden" of Unvegetated, Shallow-Water Marine Habitats. II. Role in Sediment Stability and Shallow-Water Food Webs
journal, June 1996
- Miller, Douglas C.; Geider, Richard J.; MacIntyre, Hugh L.
- Estuaries, Vol. 19, Issue 2
What is the Observed Relationship Between Species Richness and Productivity?
journal, September 2001
- Mittelbach, Gary G.; Steiner, Christopher F.; Scheiner, Samuel M.
- Ecology, Vol. 82, Issue 9
Organismal and spatial partitioning of energy and macronutrient transformations within a hypersaline mat
journal, March 2017
- Mobberley, Jennifer M.; Lindemann, Stephen R.; Bernstein, Hans C.
- FEMS Microbiology Ecology, Vol. 93, Issue 4
Spatially tracking 13 C-labelled substrate (bicarbonate) accumulation in microbial communities using laser ablation isotope ratio mass spectrometry : Spatial tracking of substrate into microbial mat
journal, October 2014
- Moran, James J.; Doll, Charles G.; Bernstein, Hans C.
- Environmental Microbiology Reports, Vol. 6, Issue 6
Cultivating Yet-to-be Cultivated Microbes: The Challenge Continues
journal, January 2013
- Narihiro, Takashi; Kamagata, Yoichi
- Microbes and Environments, Vol. 28, Issue 2
Productivity-diversity relationships from chemolithoautotrophically based sulfidic karst systems
journal, January 2009
- Porter, Megan; Summers Engel, Annette; Kane, Thomas
- International Journal of Speleology, Vol. 38, Issue 1
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
VSEARCH: a versatile open source tool for metagenomics
journal, January 2016
- Rognes, Torbjørn; Flouri, Tomáš; Nichols, Ben
- PeerJ, Vol. 4
The Continuing Puzzle of the Great Oxidation Event
journal, July 2009
- Sessions, Alex L.; Doughty, David M.; Welander, Paula V.
- Current Biology, Vol. 19, Issue 14
Microbial diversityâproductivity relationships in aquatic ecosystems: Diversityâproductivity relationships
journal, November 2007
- Smith, Val H.
- FEMS Microbiology Ecology, Vol. 62, Issue 2
Getting to the Bottom of Marine Biodiversity: Sedimentary Habitats
journal, February 1999
- Snelgrove, Paul V. R.
- BioScience, Vol. 49, Issue 2
Balance Between Autotrophic and Heterotrophic Components and Processes in Microbenthic Communities of Sandy Sediments: A Field Study
journal, December 1996
- Sundbäck, Kristina; Nilsson, Per; Nilsson, Claes
- Estuarine, Coastal and Shelf Science, Vol. 43, Issue 6
The Relationship Between Productivity and Species Richness
journal, November 1999
- Waide, R. B.; Willig, M. R.; Steiner, C. F.
- Annual Review of Ecology and Systematics, Vol. 30, Issue 1
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007
- Wang, Q.; Garrity, G. M.; Tiedje, J. M.
- Applied and Environmental Microbiology, Vol. 73, Issue 16
Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the bacterial phylum Chloroflexi
journal, June 2006
- Yamada, T.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 6
Geo- and biogeochemical processes in a heliothermal hypersaline lake
journal, May 2016
- Zachara, John M.; Moran, James J.; Resch, Charles T.
- Geochimica et Cosmochimica Acta, Vol. 181
Works referencing / citing this record:
Forfeiting the priority effect: turnover defines biofilm community succession
journal, March 2019
- Brislawn, Colin J.; Graham, Emily B.; Dana, Karl
- The ISME Journal, Vol. 13, Issue 7