Phylogenetically conserved resource partitioning in the coastal microbial loop

Bryson, Samuel; Li, Zhou; Chavez, Francisco; Weber, Peter K.; Pett-Ridge, Jennifer; Hettich, Robert L.; Pan, Chongle; Mayali, Xavier; Mueller, Ryan S.

doi:10.1038/ismej.2017.128

Phylogenetically conserved resource partitioning in the coastal microbial loop

Journal Article · Fri Aug 11 00:00:00 EDT 2017 · The ISME Journal

DOI:https://doi.org/10.1038/ismej.2017.128· OSTI ID:1394611

^[1]; Li, Zhou ^[2]; Chavez, Francisco ^[3]; Weber, Peter K. ^[4]; Pett-Ridge, Jennifer ^[4]; Hettich, Robert L. ^[2]; Pan, Chongle ^[2]; Mayali, Xavier ^[4]; Mueller, Ryan S. ^[1]

Oregon State Univ., Corvallis, OR (United States). Dept. of Microbiology
Univ. of Tennessee, Knoxville, TN (United States). Graduate School of Genome Science and Technology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Monterey Bay Aquarium Research Inst., Moss Landing, CA (United States)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)

Resource availability influences marine microbial community structure, suggesting that population-specific resource partitioning defines discrete niches. Identifying how resources are partitioned among populations, thereby characterizing functional guilds within the communities, remains a challenge for microbial ecologists. We used proteomic stable isotope probing (SIP) and NanoSIMS analysis of phylogenetic microarrays (Chip-SIP) along with 16S rRNA gene amplicon and metagenomic sequencing to characterize the assimilation of six ¹³C-labeled common metabolic substrates and changes in the microbial community structure within surface water collected from Monterey Bay, CA. Both sequencing approaches indicated distinct substrate-specific community shifts. However, observed changes in relative abundance for individual populations did not correlate well with directly measured substrate assimilation. The complementary SIP techniques identified assimilation of all six substrates by diverse taxa, but also revealed differential assimilation of substrates into protein and ribonucleotide biomass between taxa. Substrate assimilation trends indicated significantly conserved resource partitioning among populations within the Flavobacteriia, Alphaproteobacteria and Gammaproteobacteria classes, suggesting that functional guilds within marine microbial communities are phylogenetically cohesive. However, populations within these classes exhibited heterogeneity in biosynthetic activity, which distinguished high-activity copiotrophs from low-activity oligotrophs. These results indicate distinct growth responses between populations that is not apparent by genome sequencing alone.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); Oregon State Univ., Corvallis, OR (United States)

Sponsoring Organization:: Gordon and Betty Moore Foundation (United States); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC05-00OR22725; AC52-07NA27344

OSTI ID:: 1394611

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Vol. 11; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (66)

Toward Accurate and Quantitative Comparative Metagenomics Nayfach, Stephen; Pollard, Katherine S. Cell, Vol. 166, Issue 5 https://doi.org/10.1016/j.cell.2016.08.007	journal	August 2016
Large-scale analysis of the yeast proteome by multidimensional protein identification technology Washburn, Michael P.; Wolters, Dirk; Yates, John R. Nature Biotechnology, Vol. 19, Issue 3 https://doi.org/10.1038/85686	journal	March 2001
Genome characteristics of a generalist marine bacterial lineage Newton, Ryan J.; Griffin, Laura E.; Bowles, Kathy M. The ISME Journal, Vol. 4, Issue 6 https://doi.org/10.1038/ismej.2009.150	journal	January 2010
Seasonality and vertical structure of microbial communities in an ocean gyre Treusch, Alexander H.; Vergin, Kevin L.; Finlay, Liam A. The ISME Journal, Vol. 3, Issue 10 https://doi.org/10.1038/ismej.2009.60	journal	June 2009
Comparative metaproteomics reveals ocean-scale shifts in microbial nutrient utilization and energy transduction Morris, Robert M.; Nunn, Brook L.; Frazar, Christian The ISME Journal, Vol. 4, Issue 5 https://doi.org/10.1038/ismej.2010.4	journal	February 2010
High-throughput isotopic analysis of RNA microarrays to quantify microbial resource use Mayali, Xavier; Weber, Peter K.; Brodie, Eoin L. The ISME Journal, Vol. 6, Issue 6 https://doi.org/10.1038/ismej.2011.175	journal	December 2011
Phylogenetic conservatism of functional traits in microorganisms Martiny, Adam C.; Treseder, Kathleen; Pusch, Gordon The ISME Journal, Vol. 7, Issue 4 https://doi.org/10.1038/ismej.2012.160	journal	December 2012
Expression patterns reveal niche diversification in a marine microbial assemblage Gifford, Scott M.; Sharma, Shalabh; Booth, Melissa The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.96	journal	August 2012
Niches of two polysaccharide-degrading Polaribacter isolates from the North Sea during a spring diatom bloom Xing, Peng; Hahnke, Richard L.; Unfried, Frank The ISME Journal, Vol. 9, Issue 6 https://doi.org/10.1038/ismej.2014.225	journal	December 2014
Absolute quantification of microbial taxon abundances Props, Ruben; Kerckhof, Frederiek-Maarten; Rubbens, Peter The ISME Journal, Vol. 11, Issue 2 https://doi.org/10.1038/ismej.2016.117	journal	September 2016
Bacterioplankton niche partitioning in the use of phytoplankton-derived dissolved organic carbon: quantity is more important than quality Sarmento, Hugo; Morana, Cédric; Gasol, Josep M. The ISME Journal, Vol. 10, Issue 11 https://doi.org/10.1038/ismej.2016.66	journal	April 2016
Cultivation of the ubiquitous SAR11 marine bacterioplankton clade Rappé, Michael S.; Connon, Stephanie A.; Vergin, Kevin L. Nature, Vol. 418, Issue 6898 https://doi.org/10.1038/nature00917	journal	August 2002
SAR11 marine bacteria require exogenous reduced sulphur for growth Tripp, H. James; Kitner, Joshua B.; Schwalbach, Michael S. Nature, Vol. 452, Issue 7188 https://doi.org/10.1038/nature06776	journal	March 2008
Adaptive radiation by waves of gene transfer leads to fine-scale resource partitioning in marine microbes Hehemann, Jan-Hendrik; Arevalo, Philip; Datta, Manoshi S. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12860	journal	September 2016
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Stable isotope probing — linking microbial identity to function Dumont, Marc G.; Murrell, J. Colin Nature Reviews Microbiology, Vol. 3, Issue 6 https://doi.org/10.1038/nrmicro1162	journal	May 2005
Microbial structuring of marine ecosystems Azam, Farooq; Malfatti, Francesca Nature Reviews Microbiology, Vol. 5, Issue 10 https://doi.org/10.1038/nrmicro1747	journal	October 2007
Master recyclers: features and functions of bacteria associated with phytoplankton blooms Buchan, Alison; LeCleir, Gary R.; Gulvik, Christopher A. Nature Reviews Microbiology, Vol. 12, Issue 10 https://doi.org/10.1038/nrmicro3326	journal	August 2014
Annually reoccurring bacterial communities are predictable from ocean conditions Fuhrman, J. A.; Hewson, I.; Schwalbach, M. S. Proceedings of the National Academy of Sciences, Vol. 103, Issue 35 https://doi.org/10.1073/pnas.0602399103	journal	August 2006
Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea McCarren, J.; Becker, J. W.; Repeta, D. J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 38 https://doi.org/10.1073/pnas.1010732107	journal	August 2010
Microbial diversity and the lability of dissolved organic carbon Nelson, C. E.; Wear, E. K. Proceedings of the National Academy of Sciences, Vol. 111, Issue 20 https://doi.org/10.1073/pnas.1405751111	journal	May 2014
Prokaryotes: The unseen majority Whitman, W. B.; Coleman, D. C.; Wiebe, W. J. Proceedings of the National Academy of Sciences, Vol. 95, Issue 12 https://doi.org/10.1073/pnas.95.12.6578	journal	June 1998
Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments Talavera, Gerard; Castresana, Jose Systematic Biology, Vol. 56, Issue 4 https://doi.org/10.1080/10635150701472164	journal	August 2007
BamTools: a C++ API and toolkit for analyzing and managing BAM files Barnett, D. W.; Garrison, E. K.; Quinlan, A. R. Bioinformatics, Vol. 27, Issue 12 https://doi.org/10.1093/bioinformatics/btr174	journal	April 2011
Exhaustive database searching for amino acid mutations in proteomes Hyatt, Doug; Pan, Chongle Bioinformatics, Vol. 28, Issue 14 https://doi.org/10.1093/bioinformatics/bts274	journal	May 2012
Sipros/ProRata: a versatile informatics system for quantitative community proteomics Wang, Yingfeng; Ahn, Tae-Hyuk; Li, Zhou Bioinformatics, Vol. 29, Issue 16 https://doi.org/10.1093/bioinformatics/btt329	journal	June 2013
ARB: a software environment for sequence data Ludwig, W. Nucleic Acids Research, Vol. 32, Issue 4 https://doi.org/10.1093/nar/gkh293	journal	February 2004
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Community Genomics Among Stratified Microbial Assemblages in the Ocean's Interior DeLong, E. F. Science, Vol. 311, Issue 5760 https://doi.org/10.1126/science.1120250	journal	January 2006
The Genome of the Alga-Associated Marine Flavobacterium Formosa agariphila KMM 3901 ^T Reveals a Broad Potential for Degradation of Algal Polysaccharides Mann, Alexander J.; Hahnke, Richard L.; Huang, Sixing Applied and Environmental Microbiology, Vol. 79, Issue 21 https://doi.org/10.1128/aem.01937-13	journal	August 2013
Cultivation and Growth Characteristics of a Diverse Group of Oligotrophic Marine Gammaproteobacteria Cho, J. -C.; Giovannoni, S. J. Applied and Environmental Microbiology, Vol. 70, Issue 1 https://doi.org/10.1128/aem.70.1.432-440.2004	journal	January 2004
Metagenome Sequencing of a Coastal Marine Microbial Community from Monterey Bay, California Mueller, Ryan S.; Bryson, Sam; Kieft, Brandon Genome Announcements, Vol. 3, Issue 2 https://doi.org/10.1128/genomea.00341-15	journal	April 2015
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
Phylogenetic Patterns in the Microbial Response to Resource Availability: Amino Acid Incorporation in San Francisco Bay Mayali, Xavier; Weber, Peter K.; Mabery, Shalini PLoS ONE, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pone.0095842	journal	April 2014
Functional Groups of Metazoan Parasites of the Dusky Flounder (Syacium papillosum) as Bioindicators of Environmental Health of the Yucatan Shelf Vidal-Martínez, Víctor M.; Ocaña, Frank A.; Soler-Jiménez, Lilia C. Bulletin of Environmental Contamination and Toxicology https://doi.org/10.1007/s00128-021-03177-9	journal	April 2021
Linking bacterial community structure to carbon fluxes in marine environments Yokokawa, Taichi; Nagata, Toshi Journal of Oceanography, Vol. 66, Issue 1 https://doi.org/10.1007/s10872-010-0001-4	journal	January 2010
The Contribution of Monomers and other Low-Molecular Weight Compounds to the Flux of Dissolved Organic Material in Aquatic Ecosystems Kirchman, D. L. Aquatic Ecosystems https://doi.org/10.1016/B978-012256371-3/50010-X	book	January 2003
Dynamics and molecular composition of dissolved organic material during experimental phytoplankton blooms Meon, Benedikt; Kirchman, David L. Marine Chemistry, Vol. 75, Issue 3 https://doi.org/10.1016/S0304-4203(01)00036-6	journal	August 2001
The PEP—pyruvate—oxaloacetate node as the switch point for carbon flux distribution in bacteria: We dedicate this paper to Rudolf K. Thauer, Director of the Max-Planck-Institute for Terrestrial Microbiology in Marburg, Germany, on the occasion of his 65th birthday Sauer, Uwe; Eikmanns, Bernhard J. FEMS Microbiology Reviews, Vol. 29, Issue 4 https://doi.org/10.1016/j.femsre.2004.11.002	journal	September 2005
Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis Geider, Richard; La Roche, Julie European Journal of Phycology, Vol. 37, Issue 1, p. 1-17 https://doi.org/10.1017/S0967026201003456	journal	March 2002
Defining seasonal marine microbial community dynamics Gilbert, Jack A.; Steele, Joshua A.; Caporaso, J. Gregory The ISME Journal, Vol. 6, Issue 2 https://doi.org/10.1038/ismej.2011.107	journal	August 2011
Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage Dupont, Chris L.; Rusch, Douglas B.; Yooseph, Shibu The ISME Journal, Vol. 6, Issue 6 https://doi.org/10.1038/ismej.2011.189	journal	December 2011
Exploiting rRNA operon copy number to investigate bacterial reproductive strategies Roller, Benjamin R. K.; Stoddard, Steven F.; Schmidt, Thomas M. Nature Microbiology, Vol. 1, Issue 11 https://doi.org/10.1038/nmicrobiol.2016.160	journal	September 2016
Counting marine microbes with Guava Easy-Cyte 96 well plate reading flow cytometer Tripp, H. James Protocol Exchange https://doi.org/10.1038/nprot.2008.29	journal	March 2008
Coordination of microbial metabolism Chubukov, Victor; Gerosa, Luca; Kochanowski, Karl Nature Reviews Microbiology, Vol. 12, Issue 5 https://doi.org/10.1038/nrmicro3238	journal	March 2014
Detecting protein and post-translational modifications in single cells with iDentification and qUantification sEparaTion (DUET) Zhang, Yandong; Sohn, Changho; Lee, Seoyeon Communications Biology, Vol. 3, Issue 1 https://doi.org/10.1038/s42003-020-01132-8	journal	August 2020
Single bacterial strain capable of significant contribution to carbon cycling in the surface ocean Pedler, B. E.; Aluwihare, L. I.; Azam, F. Proceedings of the National Academy of Sciences, Vol. 111, Issue 20 https://doi.org/10.1073/pnas.1401887111	journal	April 2014
Quantitative Tracking of Isotope Flows in Proteomes of Microbial Communities Pan, Chongle; Fischer, Curt R.; Hyatt, Doug Molecular & Cellular Proteomics, Vol. 10, Issue 4 https://doi.org/10.1074/mcp.M110.006049	journal	February 2011
Functional and compositional succession of bacterioplankton in response to a gradient in bioavailable dissolved organic carbon: Bacterial community response to a gradient in bDOC Dinasquet, Julie; Kragh, Theis; Schrøter, Marie-Louise Environmental Microbiology, Vol. 15, Issue 9 https://doi.org/10.1111/1462-2920.12178	journal	July 2013
Taxon-specific C:N relative use efficiency for amino acids in an estuarine community Mayali, Xavier; Weber, Peter K.; Pett-Ridge, Jennifer FEMS Microbiology Ecology https://doi.org/10.1111/1574-6941.12000	journal	August 2012
Basin-scale patterns in the abundance of SAR11 subclades, marine Actinobacteria (OM1), members of the Roseobacter clade and OCS116 in the South Atlantic: Bacterioplankton communities in the South Atlantic Morris, Robert M.; Frazar, Christian D.; Carlson, Craig A. Environmental Microbiology, Vol. 14, Issue 5 https://doi.org/10.1111/j.1462-2920.2011.02694.x	journal	January 2012
Structuring of bacterioplankton communities by specific dissolved organic carbon compounds: Specialist and generalist DOC-degrading bacteria Gómez-Consarnau, Laura; Lindh, Markus V.; Gasol, Josep M. Environmental Microbiology, Vol. 14, Issue 9 https://doi.org/10.1111/j.1462-2920.2012.02804.x	journal	June 2012
Taxon-specific C/N relative use efficiency for amino acids in an estuarine community Mayali, Xavier; Weber, Peter K.; Pett-Ridge, Jennifer FEMS Microbiology Ecology, Vol. 83, Issue 2 https://doi.org/10.1111/j.1574-6941.12000.x	journal	September 2012
Substrate-Controlled Succession of Marine Bacterioplankton Populations Induced by a Phytoplankton Bloom Teeling, H.; Fuchs, B. M.; Becher, D. Science, Vol. 336, Issue 6081 https://doi.org/10.1126/science.1218344	journal	May 2012
Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform Kozich, James J.; Westcott, Sarah L.; Baxter, Nielson T. Applied and Environmental Microbiology, Vol. 79, Issue 17 https://doi.org/10.1128/AEM.01043-13	journal	June 2013
The Genome of the Alga-Associated Marine Flavobacterium Formosa agariphila KMM 3901 ^T Reveals a Broad Potential for Degradation of Algal Polysaccharides Mann, Alexander J.; Hahnke, Richard L.; Huang, Sixing Applied and Environmental Microbiology, Vol. 79, Issue 21 https://doi.org/10.1128/AEM.01937-13	journal	August 2013
Cultivation and Growth Characteristics of a Diverse Group of Oligotrophic Marine Gammaproteobacteria Cho, J. -C.; Giovannoni, S. J. Applied and Environmental Microbiology, Vol. 70, Issue 1 https://doi.org/10.1128/AEM.70.1.432-440.2004	journal	January 2004
Metagenome Sequencing of a Coastal Marine Microbial Community from Monterey Bay, California Mueller, Ryan S.; Bryson, Sam; Kieft, Brandon Genome Announcements, Vol. 3, Issue 2 https://doi.org/10.1128/genomeA.00341-15	journal	April 2015
Proteomic Stable Isotope Probing Reveals Taxonomically Distinct Patterns in Amino Acid Assimilation by Coastal Marine Bacterioplankton Bryson, Samuel; Li, Zhou; Pett-Ridge, Jennifer mSystems, Vol. 1, Issue 2 https://doi.org/10.1128/mSystems.00027-15	journal	April 2016
Application of a Database-Independent Approach To Assess the Quality of Operational Taxonomic Unit Picking Methods Schloss, Patrick D. mSystems, Vol. 1, Issue 2 https://doi.org/10.1128/mSystems.00027-16	journal	April 2016
Glycolysis for Microbiome Generation Wolfe, Alan J. Microbiology Spectrum, Vol. 3, Issue 3 https://doi.org/10.1128/microbiolspec.MBP-0014-2014	journal	June 2015
EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data Miller, Christopher S.; Baker, Brett J.; Thomas, Brian C. Genome Biology, Vol. 12, Issue 5 https://doi.org/10.1186/gb-2011-12-5-r44	journal	May 2011
Evolution and Measurement of Species Diversity Whittaker, R. H. TAXON, Vol. 21, Issue 2-3 https://doi.org/10.2307/1218190	journal	May 1972
Production and utilization of dissolved organic carbon during an experimental diatom bloom Norrman, Bo; Zwelfel, Ulla Li; Hopkinson, Charles S. Limnology and Oceanography, Vol. 40, Issue 5 https://doi.org/10.4319/lo.1995.40.5.0898	journal	July 1995
Carbon, nitrogen, and carbohydrate fluxes during the production of particulate and dissolved organic matter by marine phytoplankton Biddanda, Bopaiah; Benner, Ronald Limnology and Oceanography, Vol. 42, Issue 3 https://doi.org/10.4319/lo.1997.42.3.0506	journal	May 1997
of EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data Miller, Christopher; Baker, Brett; Thomas, Brian figshare https://doi.org/10.6084/m9.figshare.10040330.v1	image	January 2019

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