Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI

Hamilton, Joshua J.; Garcia, Sarahi L.; Brown, Brittany S.; Oyserman, Ben O.; Moya-Flores, Francisco; Bertilsson, Stefan; Malmstrom, Rex R.; Forest, Katrina T.; McMahon, Katherine D.

doi:10.1128/mSystems.00091-17

Title: Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI

Journal Article · Tue Aug 29 00:00:00 EDT 2017 · mSystems

DOI:https://doi.org/10.1128/mSystems.00091-17· OSTI ID:1459392

^[1];

^[2]; Brown, Brittany S. ^[1];

^[3]; Moya-Flores, Francisco ^[3];

^[4];

^[5]; Forest, Katrina T. ^[1];

^[6]

Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
Uppsala Univ. (Sweden). Dept. of Ecology and Genetics
Univ. of Wisconsin, Madison, WI (United States). Dept. of Civil and Environmental Engineering
Uppsala Univ. (Sweden). Dept. of Ecology and Genetics. Science for Life Lab.
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology. Dept. of Civil and Environmental Engineering

An explosion in the number of available genome sequences obtained through metagenomics and single-cell genomics has enabled a new view of the diversity of microbial life, yet we know surprisingly little about how microbes interact with each other or their environment. In fact, the majority of microbial species remain uncultivated, while our perception of their ecological niches is based on reconstruction of their metabolic potential. In this work, we demonstrate how the “seed set framework,” which computes the set of compounds that an organism must acquire from its environment (E. Borenstein, M. Kupiec, M. W. Feldman, and E. Ruppin, Proc Natl Acad Sci U S A 105:14482–14487, 2008, https://doi.org/10.1073/pnas.0806162105), enables computational analysis of metabolic reconstructions while providing new insights into a microbe’s metabolic capabilities, such as nutrient use and auxotrophies. We apply this framework to members of the ubiquitous freshwater actinobacterial lineage acI, confirming and extending previous experimental and genomic observations implying that acI bacteria are heterotrophs reliant on peptides and saccharides. We also present the first metatranscriptomic study of the acI lineage, revealing high expression of transport proteins and the light-harvesting protein actinorhodopsin. Putative transport proteins complement predictions of nutrients and essential metabolites while providing additional support of the hypothesis that members of the acI are photoheterotrophs.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA National Inst. of Food and Agriculture (NIFA); National Science Foundation (NSF); National Oceanic and Atmospheric Administration (NOAA) (United States)

Grant/Contract Number:: AC02-05CH11231; 2016-67012-24709; WIS01789; MCB-0702395; NTL-LTER DEB-1440297; DEB-1344254; NA10OAR4170070

OSTI ID:: 1459392

Journal Information:: mSystems, Vol. 2, Issue 4; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 14 works

Citation information provided by
Web of Science

References (49)

The Microbial Engines That Drive Earth's Biogeochemical Cycles Falkowski, P. G.; Fenchel, T.; Delong, E. F. Science, Vol. 320, Issue 5879 https://doi.org/10.1126/science.1153213	journal	May 2008
Toward a Predictive Understanding of Earth’s Microbiomes to Address 21st Century Challenges Blaser, Martin J.; Cardon, Zoe G.; Cho, Mildred K. mBio, Vol. 7, Issue 3 https://doi.org/10.1128/mBio.00714-16	journal	May 2016
Recovering complete and draft population genomes from metagenome datasets Sangwan, Naseer; Xia, Fangfang; Gilbert, Jack A. Microbiome, Vol. 4, Issue 1 https://doi.org/10.1186/s40168-016-0154-5	journal	March 2016
Metabolic network analysis reveals microbial community interactions in anammox granules Lawson, Christopher E.; Wu, Sha; Bhattacharjee, Ananda S. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15416	journal	May 2017
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13219	journal	October 2016
What is flux balance analysis? Orth, Jeffrey D.; Thiele, Ines; Palsson, Bernhard Ø Nature Biotechnology, Vol. 28, Issue 3 https://doi.org/10.1038/nbt.1614	journal	March 2010
Large-scale reconstruction and phylogenetic analysis of metabolic environments Borenstein, E.; Kupiec, M.; Feldman, M. W. Proceedings of the National Academy of Sciences, Vol. 105, Issue 38 https://doi.org/10.1073/pnas.0806162105	journal	September 2008
Nearly Identical 16S rRNA Sequences Recovered from Lakes in North America and Europe Indicate the Existence of Clades of Globally Distributed Freshwater Bacteria Zwart, Gabriel; Hiorns, William D.; Methé, Barbara A. Systematic and Applied Microbiology, Vol. 21, Issue 4 https://doi.org/10.1016/S0723-2020(98)80067-2	journal	December 1998
Comparative 16S rRNA Analysis of Lake Bacterioplankton Reveals Globally Distributed Phylogenetic Clusters Including an Abundant Group of Actinobacteria Glockner, F. O.; Zaichikov, E.; Belkova, N. Applied and Environmental Microbiology, Vol. 66, Issue 11 https://doi.org/10.1128/AEM.66.11.5053-5065.2000	journal	November 2000
Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers Zwart, G.; Crump, Bc; Kamst-van Agterveld, Mp Aquatic Microbial Ecology, Vol. 28 https://doi.org/10.3354/ame028141	journal	January 2002
Microbial community dynamics in a humic lake: differential persistence of common freshwater phylotypes Newton, Ryan J.; Kent, Angela D.; Triplett, Eric W. Environmental Microbiology, Vol. 8, Issue 6 https://doi.org/10.1111/j.1462-2920.2005.00979.x	journal	June 2006
Bacterioplankton Community Composition along a Salinity Gradient of Sixteen High-Mountain Lakes Located on the Tibetan Plateau, China Wu, Q. L.; Zwart, G.; Schauer, M. Applied and Environmental Microbiology, Vol. 72, Issue 8 https://doi.org/10.1128/AEM.00767-06	journal	August 2006
Phylogenetic Ecology of the Freshwater Actinobacteria acI Lineage Newton, R. J.; Jones, S. E.; Helmus, M. R. Applied and Environmental Microbiology, Vol. 73, Issue 22 https://doi.org/10.1128/AEM.00794-07	journal	September 2007
Bacterial community composition of a shallow hypertrophic freshwater lake in China, revealed by 16S rRNA gene sequences: Bacterial community of a hypertrophic freshwater lake Wu, Xin; Xi, Wanyan; Ye, Wenjin FEMS Microbiology Ecology, Vol. 61, Issue 1 https://doi.org/10.1111/j.1574-6941.2007.00326.x	journal	July 2007
Clone library analysis reveals an unusual composition and strong habitat partitioning of pelagic bacterial communities in Lake Tanganyika De Wever, A.; Van der Gucht, K.; Muylaert, K. Aquatic Microbial Ecology, Vol. 50 https://doi.org/10.3354/ame01157	journal	January 2008
Comparison of the structure and composition of bacterial communities from temperate and tropical freshwater ecosystems Humbert, Jean-F.; Dorigo, Ursula; Cecchi, Philippe Environmental Microbiology, Vol. 11, Issue 9 https://doi.org/10.1111/j.1462-2920.2009.01960.x	journal	September 2009
Breaking a paradigm: cosmopolitan and abundant freshwater actinobacteria are low GC: Freshwater actinobacteria are low GC Ghai, Rohit; McMahon, Katherine D.; Rodriguez-Valera, Francisco Environmental Microbiology Reports, Vol. 4, Issue 1 https://doi.org/10.1111/j.1758-2229.2011.00274.x	journal	August 2011
Substrate incorporation patterns of bacterioplankton populations in stratified and mixed waters of a humic lake Buck, Ulrike; Grossart, Hans-Peter; Amann, Rudolf Environmental Microbiology, Vol. 11, Issue 7 https://doi.org/10.1111/j.1462-2920.2009.01910.x	journal	July 2009
Spatiotemporal distribution and activity patterns of bacteria from three phylogenetic groups in an oligomesotrophic lake Salcher, Michaela M.; Pernthaler, Jakob; Posch, Thomas Limnology and Oceanography, Vol. 55, Issue 2 https://doi.org/10.4319/lo.2010.55.2.0846	journal	February 2010
High-throughput single-cell sequencing identifies photoheterotrophs and chemoautotrophs in freshwater bacterioplankton Martinez-Garcia, Manuel; Swan, Brandon K.; Poulton, Nicole J. The ISME Journal, Vol. 6, Issue 1 https://doi.org/10.1038/ismej.2011.84	journal	June 2011
Metabolic potential of a single cell belonging to one of the most abundant lineages in freshwater bacterioplankton Garcia, Sarahi L.; McMahon, Katherine D.; Martinez-Garcia, Manuel The ISME Journal, Vol. 7, Issue 1 https://doi.org/10.1038/ismej.2012.86	journal	July 2012
In situ substrate preferences of abundant bacterioplankton populations in a prealpine freshwater lake Salcher, Michaela M.; Posch, Thomas; Pernthaler, Jakob The ISME Journal, Vol. 7, Issue 5 https://doi.org/10.1038/ismej.2012.162	journal	December 2012
Key roles for freshwater Actinobacteria revealed by deep metagenomic sequencing Ghai, Rohit; Mizuno, Carolina Megumi; Picazo, Antonio Molecular Ecology, Vol. 23, Issue 24 https://doi.org/10.1111/mec.12985	journal	November 2014
Comparative single-cell genomics reveals potential ecological niches for the freshwater acI Actinobacteria lineage Ghylin, Trevor W.; Garcia, Sarahi L.; Moya, Francisco The ISME Journal, Vol. 8, Issue 12 https://doi.org/10.1038/ismej.2014.135	journal	August 2014
Evaluation of metatranscriptomic protocols and application to the study of freshwater microbial communities: Metatranscriptomics of freshwater communities Tsementzi, Despina; Poretsky, Rachel; Rodriguez-R, Luis M. Environmental Microbiology Reports, Vol. 6, Issue 6 https://doi.org/10.1111/1758-2229.12180	journal	June 2014
Auxotrophy and intrapopulation complementary in the ‘interactome’ of a cultivated freshwater model community Garcia, Sarahi L.; Buck, Moritz; McMahon, Katherine D. Molecular Ecology, Vol. 24, Issue 17 https://doi.org/10.1111/mec.13319	journal	August 2015
A Guide to the Natural History of Freshwater Lake Bacteria Newton, R. J.; Jones, S. E.; Eiler, A. Microbiology and Molecular Biology Reviews, Vol. 75, Issue 1 https://doi.org/10.1128/MMBR.00028-10	journal	March 2011
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes Li, L. Genome Research, Vol. 13, Issue 9 https://doi.org/10.1101/gr.1224503	journal	September 2003
Actinorhodopsins: proteorhodopsin-like gene sequences found predominantly in non-marine environments Sharma, Adrian K.; Zhaxybayeva, Olga; Papke, R. Thane Environmental Microbiology, Vol. 10, Issue 4 https://doi.org/10.1111/j.1462-2920.2007.01525.x	journal	April 2008
Uncoupling of chitinase activity and uptake of hydrolysis products in freshwater bacterioplankton Beier, Sara; Bertilsson, Stefan Limnology and Oceanography, Vol. 56, Issue 4 https://doi.org/10.4319/lo.2011.56.4.1179	journal	May 2011
Rapid successions affect microbial N-acetyl-glucosamine uptake patterns during a lacustrine spring phytoplankton bloom: Succession of NAG-consuming bacteria in a lake Eckert, Ester M.; Salcher, Michaela M.; Posch, Thomas Environmental Microbiology, Vol. 14, Issue 3 https://doi.org/10.1111/j.1462-2920.2011.02639.x	journal	November 2011
Grazing resistant freshwater bacteria profit from chitin and cell-wall-derived organic carbon: Grazing resistant pelagic scavengers Eckert, Ester M.; Baumgartner, Michael; Huber, Iris M. Environmental Microbiology, Vol. 15, Issue 7 https://doi.org/10.1111/1462-2920.12083	journal	February 2013
Contrasting ability to take up leucine and thymidine among freshwater bacterial groups: implications for bacterial production measurements PÃ©rez, MarÃa Teresa; HÃ¶rtnagl, Paul; Sommaruga, Ruben Environmental Microbiology, Vol. 12, Issue 1 https://doi.org/10.1111/j.1462-2920.2009.02043.x	journal	January 2010
The Transporter Classification Database Saier, Milton H.; Reddy, Vamsee S.; Tamang, Dorjee G. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1097	journal	November 2013
Mixed cultures as model communities: hunting for ubiquitous microorganisms, their partners, and interactions Garcia, Sl Aquatic Microbial Ecology, Vol. 77, Issue 2 https://doi.org/10.3354/ame01789	journal	August 2016
Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations Bendall, Matthew L.; Stevens, Sarah LR; Chan, Leong-Keat The ISME Journal, Vol. 10, Issue 7 https://doi.org/10.1038/ismej.2015.241	journal	January 2016
PhyloSift: phylogenetic analysis of genomes and metagenomes Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric PeerJ, Vol. 2 https://doi.org/10.7717/peerj.243	journal	January 2014
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
The large-scale organization of metabolic networks Jeong, H.; Tombor, B.; Albert, R. Nature, Vol. 407, Issue 6804 https://doi.org/10.1038/35036627	journal	October 2000
RASTtk: A modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes Brettin, Thomas; Davis, James J.; Disz, Terry Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep08365	journal	February 2015
The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST) Overbeek, Ross; Olson, Robert; Pusch, Gordon D. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1226	journal	November 2013
High-throughput generation, optimization and analysis of genome-scale metabolic models Henry, Christopher S.; DeJongh, Matthew; Best, Aaron A. Nature Biotechnology, Vol. 28, Issue 9 https://doi.org/10.1038/nbt.1672	journal	August 2010
Genomic insights that advance the species definition for prokaryotes Konstantinidis, K. T.; Tiedje, J. M. Proceedings of the National Academy of Sciences, Vol. 102, Issue 7 https://doi.org/10.1073/pnas.0409727102	journal	February 2005
HTSeq--a Python framework to work with high-throughput sequencing data Anders, S.; Pyl, P. T.; Huber, W. Bioinformatics, Vol. 31, Issue 2 https://doi.org/10.1093/bioinformatics/btu638	journal	September 2014
Mapping and quantifying mammalian transcriptomes by RNA-Seq Mortazavi, Ali; Williams, Brian A.; McCue, Kenneth Nature Methods, Vol. 5, Issue 7, p. 621-628 https://doi.org/10.1038/nmeth.1226	journal	May 2008
Reconstruction of metabolic networks from genome data and analysis of their global structure for various organisms Ma, H.; Zeng, A. -P. Bioinformatics, Vol. 19, Issue 2 https://doi.org/10.1093/bioinformatics/19.2.270	journal	January 2003
PhyloSift: Phylogenetic analysis of genomes and metagenomes Bik, Holly; Matsen, Erick; Lowe, Eric figshare https://doi.org/10.6084/m9.figshare.706369.v1	dataset	January 2013
PhyloSift: Phylogenetic analysis of genomes and metagenomes Bik, Holly; Matsen, Erick; Lowe, Eric Figshare https://doi.org/10.6084/m9.figshare.706369	dataset	January 2013

Cited By (6)

Linking metagenomics to aquatic microbial ecology and biogeochemical cycles Grossart, Hans‐Peter; Massana, Ramon; McMahon, Katherine D. Limnology and Oceanography, Vol. 65, Issue S1 https://doi.org/10.1002/lno.11382	journal	January 2020
Expansive microbial metabolic versatility and biodiversity in dynamic Guaymas Basin hydrothermal sediments Dombrowski, Nina; Teske, Andreas P.; Baker, Brett J. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07418-0	journal	November 2018
acI Actinobacteria Assemble a Functional Actinorhodopsin with Natively Synthesized Retinal Dwulit-Smith, Jeffrey R.; Hamilton, Joshua J.; Stevenson, David M. Applied and Environmental Microbiology, Vol. 84, Issue 24 https://doi.org/10.1128/aem.01678-18	journal	October 2018
Model Communities Hint at Promiscuous Metabolic Linkages between Ubiquitous Free-Living Freshwater Bacteria Garcia, Sarahi L.; Buck, Moritz; Hamilton, Joshua J. mSphere, Vol. 3, Issue 3 https://doi.org/10.1128/msphere.00202-18	journal	May 2018
Freshwater carbon and nutrient cycles revealed through reconstructed population genomes Linz, Alexandra M.; He, Shaomei; Stevens, Sarah L. R. PeerJ, Vol. 6 https://doi.org/10.7717/peerj.6075	journal	January 2018
Model communities hint at promiscuous metabolic linkages between ubiquitous free-living freshwater bacteria Garcia, Sarahi L.; Buck, Moritz; Hamilton, Joshua J. Universität Potsdam https://doi.org/10.25932/publishup-42729	text	January 2019

Similar Records

Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes

Journal Article · Wed Oct 25 00:00:00 EDT 2017 · mSphere · OSTI ID:1459392

He, Shaomei; Stevens, Sarah L. R.; Chan, Leong-Keat; +6 more

Extracellular Electron Transfer May Be an Overlooked Contribution to Pelagic Respiration in Humic-Rich Freshwater Lakes

Journal Article · Wed Jan 23 00:00:00 EST 2019 · mSphere · OSTI ID:1459392

He, Shaomei; Lau, Maximilian P.; Linz, Alexandra M.; +3 more

Genomic distribution of B-vitamin auxotrophy and uptake transporters in environmental bacteria from the Chloroflexi phylum

Journal Article · Wed Apr 01 00:00:00 EDT 2015 · Environmental Microbiology Reports, 7(2):204-210 · OSTI ID:1459392

Rodionova, Irina A.; Li, Xiaoqing; Plymale, Andrew E.; +6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
freshwater microbial ecology
metabolism
metagenomics
metatranscriptomics
physiology
systems biology

Title: Metabolic Network Analysis and Metatranscriptomics Reveal Auxotrophies and Nutrient Sources of the Cosmopolitan Freshwater Microbial Lineage acI

Citation Formats

References (49)

Cited By (6)

Similar Records

Related Subjects