Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale
Abstract
Abstract Background Biogeochemical exports from watersheds are modulated by the activity of microorganisms that function over micron scales. Here, we tested the hypothesis that meander-bound regions share a core microbiome and exhibit patterns of metabolic potential that broadly predict biogeochemical processes in floodplain soils along a river corridor. Results We intensively sampled the microbiomes of floodplain soils located in the upper, middle, and lower reaches of the East River, Colorado. Despite the very high microbial diversity and complexity of the soils, we reconstructed 248 quality draft genomes representative of subspecies. Approximately one third of these bacterial subspecies was detected across all three locations at similar abundance levels, and ~ 15% of species were detected in two consecutive years. Within the meander-bound floodplains, we did not detect systematic patterns of gene abundance based on sampling position relative to the river. However, across meanders, we identified a core floodplain microbiome that is enriched in capacities for aerobic respiration, aerobic CO oxidation, and thiosulfate oxidation with the formation of elemental sulfur. Given this, we conducted a transcriptomic analysis of the middle floodplain. In contrast to predictions made based on the prominence of gene inventories, the most highly transcribed genes were relatively rare amoCABmore »
- Authors:
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23), Climate and Environmental Sciences Division (SC-23.1)
- OSTI Identifier:
- 1784409
- Alternate Identifier(s):
- OSTI ID: 1797752
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- Microbiome
- Additional Journal Information:
- Journal Name: Microbiome Journal Volume: 9 Journal Issue: 1; Journal ID: ISSN 2049-2618
- Publisher:
- Springer Science + Business Media
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; Microbiome; Floodplain; Soil; Watershed; Genome-resolved metagenomics; Metatranscriptomics
Citation Formats
Matheus Carnevali, Paula B., Lavy, Adi, Thomas, Alex D., Crits-Christoph, Alexander, Diamond, Spencer, Méheust, Raphaël, Olm, Matthew R., Sharrar, Allison, Lei, Shufei, Dong, Wenming, Falco, Nicola, Bouskill, Nicholas, Newcomer, Michelle E., Nico, Peter, Wainwright, Haruko, Dwivedi, Dipankar, Williams, Kenneth H., Hubbard, Susan, and Banfield, Jillian F. Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale. United Kingdom: N. p., 2021.
Web. doi:10.1186/s40168-020-00957-z.
Matheus Carnevali, Paula B., Lavy, Adi, Thomas, Alex D., Crits-Christoph, Alexander, Diamond, Spencer, Méheust, Raphaël, Olm, Matthew R., Sharrar, Allison, Lei, Shufei, Dong, Wenming, Falco, Nicola, Bouskill, Nicholas, Newcomer, Michelle E., Nico, Peter, Wainwright, Haruko, Dwivedi, Dipankar, Williams, Kenneth H., Hubbard, Susan, & Banfield, Jillian F. Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale. United Kingdom. https://doi.org/10.1186/s40168-020-00957-z
Matheus Carnevali, Paula B., Lavy, Adi, Thomas, Alex D., Crits-Christoph, Alexander, Diamond, Spencer, Méheust, Raphaël, Olm, Matthew R., Sharrar, Allison, Lei, Shufei, Dong, Wenming, Falco, Nicola, Bouskill, Nicholas, Newcomer, Michelle E., Nico, Peter, Wainwright, Haruko, Dwivedi, Dipankar, Williams, Kenneth H., Hubbard, Susan, and Banfield, Jillian F. Sat .
"Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale". United Kingdom. https://doi.org/10.1186/s40168-020-00957-z.
@article{osti_1784409,
title = {Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale},
author = {Matheus Carnevali, Paula B. and Lavy, Adi and Thomas, Alex D. and Crits-Christoph, Alexander and Diamond, Spencer and Méheust, Raphaël and Olm, Matthew R. and Sharrar, Allison and Lei, Shufei and Dong, Wenming and Falco, Nicola and Bouskill, Nicholas and Newcomer, Michelle E. and Nico, Peter and Wainwright, Haruko and Dwivedi, Dipankar and Williams, Kenneth H. and Hubbard, Susan and Banfield, Jillian F.},
abstractNote = {Abstract Background Biogeochemical exports from watersheds are modulated by the activity of microorganisms that function over micron scales. Here, we tested the hypothesis that meander-bound regions share a core microbiome and exhibit patterns of metabolic potential that broadly predict biogeochemical processes in floodplain soils along a river corridor. Results We intensively sampled the microbiomes of floodplain soils located in the upper, middle, and lower reaches of the East River, Colorado. Despite the very high microbial diversity and complexity of the soils, we reconstructed 248 quality draft genomes representative of subspecies. Approximately one third of these bacterial subspecies was detected across all three locations at similar abundance levels, and ~ 15% of species were detected in two consecutive years. Within the meander-bound floodplains, we did not detect systematic patterns of gene abundance based on sampling position relative to the river. However, across meanders, we identified a core floodplain microbiome that is enriched in capacities for aerobic respiration, aerobic CO oxidation, and thiosulfate oxidation with the formation of elemental sulfur. Given this, we conducted a transcriptomic analysis of the middle floodplain. In contrast to predictions made based on the prominence of gene inventories, the most highly transcribed genes were relatively rare amoCAB and nxrAB (for nitrification) genes, followed by genes involved in methanol and formate oxidation, and nitrogen and CO 2 fixation. Within all three meanders, low soil organic carbon correlated with high activity of genes involved in methanol, formate, sulfide, hydrogen, and ammonia oxidation, nitrite oxidoreduction, and nitrate and nitrite reduction. Overall, the results emphasize the importance of sulfur, one-carbon and nitrogen compound metabolism in soils of the riparian corridor. Conclusions The disparity between the scale of a microbial cell and the scale of a watershed currently limits the development of genomically informed predictive models describing watershed biogeochemical function. Meander-bound floodplains appear to serve as scaling motifs that predict aggregate capacities for biogeochemical transformations, providing a foundation for incorporating riparian soil microbiomes in watershed models. Widely represented genetic capacities did not predict in situ activity at one time point, but rather they define a reservoir of biogeochemical potential available as conditions change.},
doi = {10.1186/s40168-020-00957-z},
journal = {Microbiome},
number = 1,
volume = 9,
place = {United Kingdom},
year = {Sat May 22 00:00:00 EDT 2021},
month = {Sat May 22 00:00:00 EDT 2021}
}
https://doi.org/10.1186/s40168-020-00957-z
Works referenced in this record:
Geochemical Exports to River From the Intrameander Hyporheic Zone Under Transient Hydrologic Conditions: East River Mountainous Watershed, Colorado
journal, October 2018
- Dwivedi, Dipankar; Steefel, Carl I.; Arora, Bhavna
- Water Resources Research, Vol. 54, Issue 10
UFBoot2: Improving the Ultrafast Bootstrap Approximation
journal, October 2017
- Hoang, Diep Thi; Chernomor, Olga; von Haeseler, Arndt
- Molecular Biology and Evolution, Vol. 35, Issue 2
Associations between species and groups of sites: indices and statistical inference
journal, December 2009
- Cáceres, Miquel De; Legendre, Pierre
- Ecology, Vol. 90, Issue 12
The ade4 Package: Implementing the Duality Diagram for Ecologists
journal, January 2007
- Dray, Stéphane; Dufour, Anne-Béatrice
- Journal of Statistical Software, Vol. 22, Issue 4
Improved testing of species traits–environment relationships in the fourth-corner problem
journal, July 2012
- ter Braak, Cajo J. F.; Cormont, Anouk; Dray, Stéphane
- Ecology, Vol. 93, Issue 7
Combining the fourth-corner and the RLQ methods for assessing trait responses to environmental variation
journal, January 2014
- Dray, Stéphane; Choler, Philippe; Dolédec, Sylvain
- Ecology, Vol. 95, Issue 1
Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria
journal, January 2019
- Matheus Carnevali, Paula B.; Schulz, Frederik; Castelle, Cindy J.
- Nature Communications, Vol. 10, Issue 1
dbCAN2: a meta server for automated carbohydrate-active enzyme annotation
journal, May 2018
- Zhang, Han; Yohe, Tanner; Huang, Le
- Nucleic Acids Research, Vol. 46, Issue W1
KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 2000
- Kanehisa, Minoru; Goto, Susumu
- Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30
Atmospheric carbon monoxide oxidation is a widespread mechanism supporting microbial survival
journal, July 2019
- Cordero, Paul R. F.; Bayly, Katherine; Man Leung, Pok
- The ISME Journal, Vol. 13, Issue 11
Contrasting the hydrologic response due to land cover and climate change in a mountain headwaters system: Contrasting hydrologic response from land cover and climate change
journal, September 2016
- Pribulick, Christine E.; Foster, Lauren M.; Bearup, Lindsay A.
- Ecohydrology, Vol. 9, Issue 8
Comparison of Burrows-Wheeler Transform-Based Mapping Algorithms Used in High-Throughput Whole-Genome Sequencing: Application to Illumina Data for Livestock Genomes1
journal, February 2018
- Keel, Brittney N.; Snelling, Warren M.
- Frontiers in Genetics, Vol. 9
Distribution, diversity and ecology of aerobic CO-oxidizing bacteria
journal, February 2007
- King, Gary M.; Weber, Carolyn F.
- Nature Reviews Microbiology, Vol. 5, Issue 2
De novo clustering methods outperform reference-based methods for assigning 16S rRNA gene sequences to operational taxonomic units
journal, January 2015
- Westcott, Sarah L.; Schloss, Patrick D.
- PeerJ, Vol. 3
Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010
- Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F.
- BMC Bioinformatics, Vol. 11, Issue 1
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities
journal, January 2015
- Kang, Dongwan D.; Froula, Jeff; Egan, Rob
- PeerJ, Vol. 3
Land-use influences the distribution and activity of high affinity CO-oxidizing bacteria associated to type I-coxL genotype in soil
journal, June 2014
- Quiza, Liliana; Lalonde, Isabelle; Guertin, Claude
- Frontiers in Microbiology, Vol. 5
MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets
journal, October 2015
- Wu, Yu-Wei; Simmons, Blake A.; Singer, Steven W.
- Bioinformatics, Vol. 32, Issue 4
Assessment of the importance of dissimilatory nitrate reduction to ammonium for the terrestrial nitrogen cycle
journal, January 2011
- Rütting, T.; Boeckx, P.; Müller, C.
- Biogeosciences, Vol. 8, Issue 7
HMMER Cut-off Threshold Tool (HMMERCTTER): Supervised classification of superfamily protein sequences with a reliable cut-off threshold
journal, March 2018
- Pagnuco, Inti Anabela; Revuelta, María Victoria; Bondino, Hernán Gabriel
- PLOS ONE, Vol. 13, Issue 3
KofamKOALA: KEGG ortholog assignment based on profile HMM and adaptive score threshold
posted_content, April 2019
- Aramaki, Takuya; Blanc-Mathieu, Romain; Endo, Hisashi
- Bioinformatics
PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference
journal, May 2014
- Keltjens, Jan T.; Pol, Arjan; Reimann, Joachim
- Applied Microbiology and Biotechnology, Vol. 98, Issue 14
The East River, Colorado, Watershed: A Mountainous Community Testbed for Improving Predictive Understanding of Multiscale Hydrological–Biogeochemical Dynamics
journal, January 2018
- Hubbard, Susan S.; Williams, Kenneth Hurst; Agarwal, Deb
- Vadose Zone Journal, Vol. 17, Issue 1
Functional Diversity of Carbohydrate-Active Enzymes Enabling a Bacterium to Ferment Plant Biomass
journal, November 2014
- Boutard, Magali; Cerisy, Tristan; Nogue, Pierre-Yves
- PLoS Genetics, Vol. 10, Issue 11
Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy
journal, May 2018
- Sieber, Christian M. K.; Probst, Alexander J.; Sharrar, Allison
- Nature Microbiology, Vol. 3, Issue 7
IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth
journal, April 2012
- Peng, Y.; Leung, H. C. M.; Yiu, S. M.
- Bioinformatics, Vol. 28, Issue 11
Fermentation of pectin and glucose, and activity of pectin-degrading enzymes in the rumen bacterium Lachnospira multiparus
journal, August 2001
- Duskova, D.; Marounek, M.
- Letters in Applied Microbiology, Vol. 33, Issue 2
Complex response of the forest nitrogen cycle to climate change
journal, February 2012
- Bernal, S.; Hedin, L. O.; Likens, G. E.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 9
Microbial communities across a hillslope‐riparian transect shaped by proximity to the stream, groundwater table, and weathered bedrock
journal, May 2019
- Lavy, Adi; McGrath, David Geller; Matheus Carnevali, Paula B.
- Ecology and Evolution, Vol. 9, Issue 12
Mediterranean grassland soil C–N compound turnover is dependent on rainfall and depth, and is mediated by genomically divergent microorganisms
journal, May 2019
- Diamond, Spencer; Andeer, Peter F.; Li, Zhou
- Nature Microbiology, Vol. 4, Issue 8
ModelFinder: fast model selection for accurate phylogenetic estimates
journal, May 2017
- Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F.
- Nature Methods, Vol. 14, Issue 6
The rise of diversity in metabolic platforms across the Candidate Phyla Radiation
journal, June 2020
- Jaffe, Alexander L.; Castelle, Cindy J.; Matheus Carnevali, Paula B.
- BMC Biology, Vol. 18, Issue 1
UniProt: a worldwide hub of protein knowledge
November 2018
- Consortium, The UniProt
- Nucleic Acids Research
Unusual biology across a group comprising more than 15% of domain Bacteria
journal, June 2015
- Brown, Christopher T.; Hug, Laura A.; Thomas, Brian C.
- Nature, Vol. 523, Issue 7559
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009
- Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T.
- Bioinformatics, Vol. 25, Issue 15
Binning metagenomic contigs by coverage and composition
journal, September 2014
- Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino
- Nature Methods, Vol. 11, Issue 11
The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013
- Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
- Nucleic Acids Research, Vol. 42, Issue D1
A complete domain-to-species taxonomy for Bacteria and Archaea
journal, April 2020
- Parks, Donovan H.; Chuvochina, Maria; Chaumeil, Pierre-Alain
- Nature Biotechnology
Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes
journal, May 2013
- Albertsen, Mads; Hugenholtz, Philip; Skarshewski, Adam
- Nature Biotechnology, Vol. 31, Issue 6
Fast gapped-read alignment with Bowtie 2
journal, March 2012
- Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 9, Issue 4
Creating the CIPRES Science Gateway for inference of large phylogenetic trees
conference, November 2010
- Miller, Mark A.; Pfeiffer, Wayne; Schwartz, Terri
- 2010 Gateway Computing Environments Workshop (GCE)
dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication
journal, July 2017
- Olm, Matthew R.; Brown, Christopher T.; Brooks, Brandon
- The ISME Journal, Vol. 11, Issue 12
XoxF encoding an alternative methanol dehydrogenase is widespread in coastal marine environments
journal, June 2015
- Taubert, Martin; Grob, Carolina; Howat, Alexandra M.
- Environmental Microbiology, Vol. 17, Issue 10
Water table elevation controls on soil nitrogen cycling in riparian wetlands along a European climatic gradient
journal, January 2004
- Hefting, M.; Clément, J. C.; Dowrick, D.
- Biogeochemistry, Vol. 67, Issue 1
Microbial Community Functional Potential and Composition Are Shaped by Hydrologic Connectivity in Riverine Floodplain Soils
journal, November 2016
- Argiroff, William A.; Zak, Donald R.; Lanser, Christine M.
- Microbial Ecology, Vol. 73, Issue 3
Groundwater Elusimicrobia are metabolically diverse compared to gut microbiome Elusimicrobia and some have a novel nitrogenase paralog
journal, July 2020
- Méheust, Raphaël; Castelle, Cindy J.; Matheus Carnevali, Paula B.
- The ISME Journal, Vol. 14, Issue 12
A simple method to control over-alignment in the MAFFT multiple sequence alignment program
journal, February 2016
- Katoh, Kazutaka; Standley, Daron M.
- Bioinformatics, Vol. 32, Issue 13
Convergent evidence for widespread rock nitrogen sources in Earth’s surface environment
journal, April 2018
- Houlton, B. Z.; Morford, S. L.; Dahlgren, R. A.
- Science, Vol. 360, Issue 6384
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system
journal, October 2016
- Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A.
- Nature Communications, Vol. 7, Issue 1
The Problem of Pattern and Scale in Ecology: The Robert H. MacArthur Award Lecture
journal, December 1992
- Levin, Simon A.
- Ecology, Vol. 73, Issue 6
Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi)sulfite reductases
journal, October 2014
- Müller, Albert Leopold; Kjeldsen, Kasper Urup; Rattei, Thomas
- The ISME Journal, Vol. 9, Issue 5
Predicting sedimentary bedrock subsurface weathering fronts and weathering rates
journal, November 2019
- Wan, Jiamin; Tokunaga, Tetsu K.; Williams, Kenneth H.
- Scientific Reports, Vol. 9, Issue 1
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12
Importance and vulnerability of the world’s water towers
journal, December 2019
- Immerzeel, W. W.; Lutz, A. F.; Andrade, M.
- Nature, Vol. 577, Issue 7790
Snowmelt controls on concentration-discharge relationships and the balance of oxidative and acid-base weathering fluxes in an alpine catchment, East River, Colorado: ACID-BASE VERSUS OXIDATIVE WEATHERING FLUXES
journal, March 2017
- Winnick, Matthew J.; Carroll, Rosemary W. H.; Williams, Kenneth H.
- Water Resources Research, Vol. 53, Issue 3