Metatranscriptomic insights on gene expression and regulatory controls in Candidatus Accumulibacter phosphatis

Oyserman, Ben O.; Noguera, Daniel R.; del Rio, Tijana Glavina; Tringe, Susannah G.; McMahon, Katherine D.

doi:10.1038/ismej.2015.155

Title: Metatranscriptomic insights on gene expression and regulatory controls in Candidatus Accumulibacter phosphatis

Journal Article · Tue Nov 10 00:00:00 EST 2015 · The ISME Journal

DOI:https://doi.org/10.1038/ismej.2015.155· OSTI ID:1346927

Oyserman, Ben O. ^[1]; Noguera, Daniel R. ^[1]; del Rio, Tijana Glavina ^[2];

^[2]; McMahon, Katherine D. ^[1]

Univ. of Wisconsin, Madison, WI (United States)
U.S. Dept. of Energy Joint Genome Institute, Walnut Creek, CA (United States)

© 2016 International Society for Microbial Ecology All rights reserved. Previous studies on enhanced biological phosphorus removal (EBPR) have focused on reconstructing genomic blueprints for the model polyphosphate-accumulating organism Candidatus Accumulibacter phosphatis. Here, a time series metatranscriptome generated from enrichment cultures of Accumulibacter was used to gain insight into anerobic/aerobic metabolism and regulatory mechanisms within an EBPR cycle. Co-expressed gene clusters were identified displaying ecologically relevant trends consistent with batch cycle phases. Transcripts displaying increased abundance during anerobic acetate contact were functionally enriched in energy production and conversion, including upregulation of both cytoplasmic and membrane-bound hydrogenases demonstrating the importance of transcriptional regulation to manage energy and electron flux during anerobic acetate contact. We hypothesized and demonstrated hydrogen production after anerobic acetate contact, a previously unknown strategy for Accumulibacter to maintain redox balance. Genes involved in anerobic glycine utilization were identified and phosphorus release after anerobic glycine contact demonstrated, suggesting that Accumulibacter routes diverse carbon sources to acetyl-CoA formation via previously unrecognized pathways. A comparative genomics analysis of sequences upstream of co-expressed genes identified two statistically significant putative regulatory motifs. One palindromic motif was identified upstream of genes involved in PHA synthesis and acetate activation and is hypothesized to be a phaR binding site, hence representing a hypothetical PHA modulon. A second motif was identified ~35 base pairs (bp) upstream of a large and diverse array of genes and hence may represent a sigma factor bind ing site. This analysis provides a basis and framework for further investigations into Accumulibacter metabolism and the reconstruction of regulatory networks in uncultured organisms.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1346927

Alternate ID(s):: OSTI ID: 1379256

Journal Information:: The ISME Journal, Vol. 10, Issue 4; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 64 works

Citation information provided by
Web of Science

References (64)

Identification of Polyphosphate-Accumulating Organisms and Design of 16S rRNA-Directed Probes for Their Detection and Quantitation Crocetti, G. R.; Hugenholtz, P.; Bond, P. L. Applied and Environmental Microbiology, Vol. 66, Issue 3 https://doi.org/10.1128/AEM.66.3.1175-1182.2000	journal	March 2000
‘Candidatus Accumulibacter’ gene expression in response to dynamic EBPR conditions He, Shaomei; McMahon, Katherine D. The ISME Journal, Vol. 5, Issue 2 https://doi.org/10.1038/ismej.2010.127	journal	August 2010
Polyhydroxyalkanoates: an overview Reddy, C. S. K.; Ghai, R. Bioresource Technology, Vol. 87, Issue 2, p. 137-146 https://doi.org/10.1016/s0960-8524(02)00212-2	journal	April 2003
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
Principles of transcriptional regulation and evolution of the metabolic system in E. coli Seshasayee, A. S. N.; Fraser, G. M.; Babu, M. M. Genome Research, Vol. 19, Issue 1 https://doi.org/10.1101/gr.079715.108	journal	October 2008
Crystal Structure of the "PhoU-Like" Phosphate Uptake Regulator from Aquifex aeolicus Oganesyan, V.; Oganesyan, N.; Adams, P. D. Journal of Bacteriology, Vol. 187, Issue 12 https://doi.org/10.1128/jb.187.12.4238-4244.2005	journal	June 2005
Cost-Benefit Tradeoffs in Engineered lac Operons Eames, M.; Kortemme, T. Science, Vol. 336, Issue 6083 https://doi.org/10.1126/science.1219083	journal	May 2012
Anaerobic metabolism of bacteria performing enhanced biological phosphate removal Hesselmann, R. Water Research, Vol. 34, Issue 14 https://doi.org/10.1016/S0043-1354(00)00092-0	journal	October 2000
Community proteogenomics highlights microbial strain-variant protein expression within activated sludge performing enhanced biological phosphorus removal Wilmes, Paul; Andersson, Anders F.; Lefsrud, Mark G. The ISME Journal, Vol. 2, Issue 8 https://doi.org/10.1038/ismej.2008.38	journal	May 2008
Development of a revised metabolic model for the growth of phosphorus-accumulating organisms Filipe, Carlos D. M.; Daigger, Glen T. Water Environment Research, Vol. 70, Issue 1 https://doi.org/10.2175/106143098X126900	journal	January 1998
Involvement of the TCA cycle in the anaerobic metabolism of polyphosphate accumulating organisms (PAOs) Zhou, Yan; Pijuan, Maite; Zeng, Raymond J. Water Research, Vol. 43, Issue 5 https://doi.org/10.1016/j.watres.2008.12.008	journal	March 2009
Proton motive force generation from stored polymers for the uptake of acetate under anaerobic conditions Saunders, Aaron M.; Mabbett, Amanda N.; McEwan, Alastair G. FEMS Microbiology Letters, Vol. 274, Issue 2 https://doi.org/10.1111/j.1574-6968.2007.00839.x	journal	September 2007
Regulation of phasin expression and polyhydroxyalkanoate (PHA) granule formation in Ralstonia eutropha H16 Pötter, Markus; Madkour, Mohamed H.; Mayer, Frank Microbiology, Vol. 148, Issue 8 https://doi.org/10.1099/00221287-148-8-2413	journal	August 2002
Engineering a Cyanobacterial Cell Factory for Production of Lactic Acid Angermayr, S. Andreas; Paszota, Michal; Hellingwerf, Klaas J. Applied and Environmental Microbiology, Vol. 78, Issue 19 https://doi.org/10.1128/AEM.01587-12	journal	August 2012
Biological Aspects of Inorganic Polyphosphates Wood, Harland G.; Clark, Joan E. Annual Review of Biochemistry, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.bi.57.070188.001315	journal	June 1988
Glycine metabolism in anaerobes Andreesen, Jan R. Antonie van Leeuwenhoek, Vol. 66, Issue 1-3 https://doi.org/10.1007/BF00871641	journal	January 1994
Refined DNase-seq protocol and data analysis reveals intrinsic bias in transcription factor footprint identification He, Housheng Hansen; Meyer, Clifford A.; Hu, Sheng'en Shawn Nature Methods, Vol. 11, Issue 1 https://doi.org/10.1038/nmeth.2762	journal	December 2013
Combining evidence using p-values: application to sequence homology searches Bailey, T. L.; Gribskov, M. Bioinformatics, Vol. 14, Issue 1 https://doi.org/10.1093/bioinformatics/14.1.48	journal	February 1998
Comparative genomics of two ‘Candidatus Accumulibacter’ clades performing biological phosphorus removal Flowers, Jason J.; He, Shaomei; Malfatti, Stephanie The ISME Journal, Vol. 7, Issue 12 https://doi.org/10.1038/ismej.2013.117	journal	July 2013
Genome Reconstruction and Gene Expression of “ Candidatus Accumulibacter phosphatis” Clade IB Performing Biological Phosphorus Removal Mao, Yanping; Yu, Ke; Xia, Yu Environmental Science & Technology, Vol. 48, Issue 17 https://doi.org/10.1021/es502642b	journal	August 2014
Analysis of E.Coli Pormoter sequences Harley, Calvin B.; Reynolds, Robert P. Nucleic Acids Research, Vol. 15, Issue 5 https://doi.org/10.1093/nar/15.5.2343	journal	January 1987
Cloning and nucleotide sequence of the gcv operon encoding the Escherichia coli glycine-cleavage system Okamura-Ikeda, Kazuko; Ohmura, Yosuke; Fujiwara, Kazuko European Journal of Biochemistry, Vol. 216, Issue 2 https://doi.org/10.1111/j.1432-1033.1993.tb18172.x	journal	September 1993
The Cost of Expression of Escherichia coli lac Operon Proteins Is in the Process, Not in the Products Stoebel, Daniel M.; Dean, Antony M.; Dykhuizen, Daniel E. Genetics, Vol. 178, Issue 3 https://doi.org/10.1534/genetics.107.085399	journal	February 2008
SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data Kopylova, Evguenia; Noé, Laurent; Touzet, Hélène Bioinformatics, Vol. 28, Issue 24 https://doi.org/10.1093/bioinformatics/bts611	journal	October 2012
Crystal structure of (R)-3-hydroxybutyryl-CoA dehydrogenase PhaB from Ralstonia eutropha Kim, Jieun; Chang, Jeong Ho; Kim, Eun-Jung Biochemical and Biophysical Research Communications, Vol. 443, Issue 3 https://doi.org/10.1016/j.bbrc.2013.10.150	journal	January 2014
Molecular basis for biosynthesis and accumulation of polyhydroxyalkanoic acids in bacteria SteinbÃ¼chel, A.; Hustede, E.; Liebergesell, M. FEMS Microbiology Letters, Vol. 103, Issue 2-4 https://doi.org/10.1111/j.1574-6968.1992.tb05841.x	journal	December 1992
MEME SUITE: tools for motif discovery and searching Bailey, T. L.; Boden, M.; Buske, F. A. Nucleic Acids Research, Vol. 37, Issue Web Server https://doi.org/10.1093/nar/gkp335	journal	May 2009
Microbial communities involved in enhanced biological phosphorus removal from wastewater—a model system in environmental biotechnology Nielsen, Per Halkjær; Saunders, Aaron Marc; Hansen, Aviaja Anna Current Opinion in Biotechnology, Vol. 23, Issue 3 https://doi.org/10.1016/j.copbio.2011.11.027	journal	June 2012
Footprinting: A method for determining the sequence selectivity, affinity and kinetics of DNA-binding ligands Hampshire, A.; Rusling, D.; Broughtonhead, V. Methods, Vol. 42, Issue 2 https://doi.org/10.1016/j.ymeth.2007.01.002	journal	June 2007
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
Transcript and protein level analyses of the interactions among PhoB, PhoR, PhoU and CreC in response to phosphate starvation in Escherichia coli Baek, Jong Hwan; Kang, Yeon Jae; Lee, Sang Yup FEMS Microbiology Letters, Vol. 277, Issue 2 https://doi.org/10.1111/j.1574-6968.2007.00965.x	journal	December 2007
Metaproteomics Provides Functional Insight into Activated Sludge Wastewater Treatment Wilmes, Paul; Wexler, Margaret; Bond, Philip L. PLoS ONE, Vol. 3, Issue 3 https://doi.org/10.1371/journal.pone.0001778	journal	March 2008
Crystal Structure of a PhoU Protein Homologue: A NEW CLASS OF METALLOPROTEIN CONTAINING MULTINUCLEAR IRON CLUSTERS Liu, Jinyu; Lou, Yun; Yokota, Hisao Journal of Biological Chemistry, Vol. 280, Issue 16 https://doi.org/10.1074/jbc.M414117200	journal	February 2005
Long-chain acyl-CoA synthetases and fatty acid channeling Rosalind, Coleman,; Lei, Li,; Douglas, Mashek, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/m2ht-p111	text	January 2007
Denitrification capabilities of two biological phosphorus removal sludges dominated by different â€˜ Candidatus Accumulibacterâ€™ clades Flowers, Jason J.; He, Shaomei; Yilmaz, Safak Environmental Microbiology Reports, Vol. 1, Issue 6 https://doi.org/10.1111/j.1758-2229.2009.00090.x	journal	December 2009
Java Treeview--extensible visualization of microarray data Saldanha, A. J. Bioinformatics, Vol. 20, Issue 17 https://doi.org/10.1093/bioinformatics/bth349	journal	June 2004
Incorporating microbial ecology into the metabolic modelling of polyphosphate accumulating organisms and glycogen accumulating organisms Oehmen, A.; Carvalho, G.; Lopez-Vazquez, C. M. Water Research, Vol. 44, Issue 17 https://doi.org/10.1016/j.watres.2010.06.071	journal	September 2010
Biochemical model for enhanced biological phosphorus removal Comeau, Y.; Hall, K.; Hancock, R. Water Research, Vol. 20, Issue 12 https://doi.org/10.1016/0043-1354(86)90115-6	journal	December 1986
Characterization of the Carboxysomal Carbonic Anhydrase CsoSCA from Halothiobacillus neapolitanus Heinhorst, S.; Williams, E. B.; Cai, F. Journal of Bacteriology, Vol. 188, Issue 23 https://doi.org/10.1128/JB.00990-06	journal	September 2006
Enrichment, Phylogenetic Analysis and Detection of a Bacterium That Performs Enhanced Biological Phosphate Removal in Activated Sludge Hesselmann, Rolf P. X.; Werlen, Christoph; Hahn, Dittmar Systematic and Applied Microbiology, Vol. 22, Issue 3 https://doi.org/10.1016/S0723-2020(99)80055-1	journal	September 1999
Long-chain acyl-CoA synthetases and fatty acid channeling Mashek, Douglas G.; Li, Lei O.; Coleman, Rosalind A. Future Lipidology, Vol. 2, Issue 4 https://doi.org/10.2217/17460875.2.4.465	journal	August 2007
Global Analysis of Photosynthesis Transcriptional Regulatory Networks Imam, Saheed; Noguera, Daniel R.; Donohue, Timothy J. PLoS Genetics, Vol. 10, Issue 12 https://doi.org/10.1371/journal.pgen.1004837	journal	December 2014
Microbiology and biochemistry of the enhanced biological phosphate removal process Mino, T.; van Loosdrecht, M. C. M.; Heijnen, J. J. Water Research, Vol. 32, Issue 11 https://doi.org/10.1016/S0043-1354(98)00129-8	journal	November 1998
Candidatus Accumulibacter phosphatis: Elusive Bacterium Responsible for Enhanced Biological Phosphorus Removal Kang, Dae-Wook; Noguera, Daniel R. Journal of Environmental Engineering, Vol. 140, Issue 1 https://doi.org/10.1061/(ASCE)EE.1943-7870.0000781	journal	January 2014
Determination of Poly-β-Hydroxybutyrate and Poly-β-Hydroxyvalerate in Activated Sludge by Gas-Liquid Chromatography Comeau, Yves; Hall, Kenneth J.; Oldham, William K. Applied and Environmental Microbiology, Vol. 54, Issue 9 https://doi.org/10.1128/AEM.54.9.2325-2327.1988	journal	January 1988
Metabolic Engineering of Poly(3-Hydroxyalkanoates): From DNA to Plastic Madison, Lara L.; Huisman, Gjalt W. Microbiology and Molecular Biology Reviews, Vol. 63, Issue 1 https://doi.org/10.1128/MMBR.63.1.21-53.1999	journal	January 1999
Radiolabelled proteomics to determine differential functioning of Accumulibacter during the anaerobic and aerobic phases of a bioreactor operating for enhanced biological phosphorus removal Wexler, Margaret; Richardson, David J.; Bond, Philip L. Environmental Microbiology, Vol. 11, Issue 12 https://doi.org/10.1111/j.1462-2920.2009.02007.x	journal	December 2009
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
Enzymology, genetics, and regulation of membrane phospholipid synthesis in Escherichia coli Raetz, C. R. Microbiological Reviews, Vol. 42, Issue 3 https://doi.org/10.1128/mr.42.3.614-659.1978	journal	September 1978
Bacterial community structures of phosphate-removing and non-phosphate-removing activated sludges from sequencing batch reactors. Bond, P. L.; Hugenholtz, P.; Keller, J. Applied and environmental microbiology, Vol. 61, Issue 5 https://doi.org/10.1128/aem.61.5.1910-1916.1995	journal	January 1995
The group A streptococcal collagen-like protein-1, Scl1, mediates biofilm formation by targeting the extra domain A-containing variant of cellular fibronectin expressed in wounded tissue: Scl1 binding to cellular fibronectin Oliver-Kozup, Heaven; Martin, Karen H.; Schwegler-Berry, Diane Molecular Microbiology, Vol. 87, Issue 3 https://doi.org/10.1111/mmi.12125	journal	December 2012
The strong efficiency of the Escherichia coli gapA P1 promoter depends on a complex combination of functional determinants Thouvenot, Benoit; Charpentier, Bruno; Branlant, Christiane Biochemical Journal, Vol. 383, Issue 2 https://doi.org/10.1042/bj20040792	journal	October 2004
Intermediary Metabolism of Diplococcus Glycinophilus i. Sagers, Richard D.; Gunsalus, I. C. Journal of Bacteriology, Vol. 81, Issue 4 https://doi.org/10.1128/JB.81.4.541-549.1961	journal	January 1961
The streptococcal collagen-like protein-1 (Scl1) is a significant determinant for biofilm formation by group A Streptococcus Oliver-Kozup, Heaven A.; Elliott, Meenal; Bachert, Beth A. BMC Microbiology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2180-11-262	journal	January 2011
Sequencing and comparison of yeast species to identify genes and regulatory elements Kellis, Manolis; Patterson, Nick; Endrizzi, Matthew Nature, Vol. 423, Issue 6937 https://doi.org/10.1038/nature01644	journal	May 2003
Engineering Cyanobacteria To Synthesize and Export Hydrophilic Products Niederholtmeyer, H.; Wolfstadter, B. T.; Savage, D. F. Applied and Environmental Microbiology, Vol. 76, Issue 11 https://doi.org/10.1128/AEM.00202-10	journal	April 2010
Polyhydroxyalkanoate Granules Are Complex Subcellular Organelles (Carbonosomes) Jendrossek, D. Journal of Bacteriology, Vol. 191, Issue 10 https://doi.org/10.1128/JB.01723-08	journal	March 2009
Enzymology, genetics, and regulation of membrane phospholipid synthesis in Escherichia coli. Raetz, C. R. Microbiological Reviews, Vol. 42, Issue 3 https://doi.org/10.1128/MMBR.42.3.614-659.1978	journal	January 1978
Persistence of adoptively transferred T cells with a kinetically engineered IL-2 receptor agonist Parisi, Giulia; Saco, Justin D.; Salazar, Felix B. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-019-12901-3	journal	January 2020
Metatranscriptomic array analysis of ‘Candidatus Accumulibacter phosphatis’-enriched enhanced biological phosphorus removal sludge: Metatranscriptomic array analysis of EBPR sludge He, Shaomei; Kunin, Victor; Haynes, Matthew Environmental Microbiology, Vol. 12, Issue 5 https://doi.org/10.1111/j.1462-2920.2010.02163.x	journal	February 2010
Bacterial collagen-like proteins that form triple-helical structures Yu, Zhuoxin; An, Bo; Ramshaw, John A. M. Journal of Structural Biology, Vol. 186, Issue 3 https://doi.org/10.1016/j.jsb.2014.01.003	journal	June 2014
Metagenomic analysis of two enhanced biological phosphorus removal (EBPR) sludge communities Martín, Héctor García; Ivanova, Natalia; Kunin, Victor Nature Biotechnology, Vol. 24, Issue 10 https://doi.org/10.1038/nbt1247	journal	September 2006
Expanding our view of genomic diversity in C andidatus Accumulibacter clades : Metabolic plasticity in Accumulibacter clades Skennerton, Connor T.; Barr, Jeremy J.; Slater, Frances R. Environmental Microbiology, Vol. 17, Issue 5 https://doi.org/10.1111/1462-2920.12582	journal	August 2014
Poly-β-hydroxybutyrate (PHB) biosynthesis in Alcaligenes eutrophus H16 Peoples, O. P.; Sinskey, A. J. Journal of Biological Chemistry, Vol. 264, Issue 26 https://doi.org/10.1016/S0021-9258(19)84825-1	journal	September 1989

Cited By (17)

Compositional variation between high and low prokaryotic diversity coral reef biotopes translates to different predicted metagenomic gene content Cleary, Daniel F. R.; Polónia, Ana Rita M.; Huang, Yusheng M. Antonie van Leeuwenhoek, Vol. 113, Issue 4 https://doi.org/10.1007/s10482-019-01364-7	journal	December 2019
Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil Yao, Qiuming; Li, Zhou; Song, Yang Nature Ecology & Evolution, Vol. 2, Issue 3 https://doi.org/10.1038/s41559-017-0463-5	journal	January 2018
Cyclic Metabolism as a Mode of Microbial Existence Dorofeev, A. G.; Nikolaev, Yu. A.; Mardanov, A. V. Microbiology, Vol. 88, Issue 4 https://doi.org/10.1134/s0026261719040052	journal	July 2019
Revealing metabolic flexibility of Candidatus Accumulibacter phosphatis through redox cofactor analysis and metabolic network modeling da Silva, Leonor Guedes; Gamez, Karel Olavarria; Gomes, Joana Castro BioRxiv https://doi.org/10.1101/458331	posted_content	March 2019
Genomic and in Situ Analyses Reveal the Micropruina spp. as Abundant Fermentative Glycogen Accumulating Organisms in Enhanced Biological Phosphorus Removal Systems McIlroy, Simon J.; Onetto, Cristobal A.; McIlroy, Bianca Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01004	journal	May 2018
Integrated Omic Analyses Provide Evidence that a “Candidatus Accumulibacter phosphatis” Strain Performs Denitrification under Microaerobic Conditions Camejo, Pamela Y.; Oyserman, Ben O.; McMahon, Katherine D. mSystems, Vol. 4, Issue 1 https://doi.org/10.1128/msystems.00193-18	journal	January 2019
Spatiotemporal heterogeneity of core functional bacteria and their synergetic and competitive interactions in denitrifying sulfur conversion-assisted enhanced biological phosphorus removal Zhang, Yan; Yu, Mei; Guo, Jianhua Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-11448-x	journal	September 2017
Archaeal communities in sponge, sediment and water from marine lakes and open water habitats Polónia, Ana Rita Moura; Cleary, Daniel Francis Richard Marine Biology Research, Vol. 15, Issue 3 https://doi.org/10.1080/17451000.2019.1633469	journal	March 2019
A Critical Assessment of the Microorganisms Proposed to be Important to Enhanced Biological Phosphorus Removal in Full-Scale Wastewater Treatment Systems Stokholm-Bjerregaard, Mikkel; McIlroy, Simon J.; Nierychlo, Marta Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00718	journal	April 2017
“Candidatus Propionivibrio aalborgensis”: A Novel Glycogen Accumulating Organism Abundant in Full-Scale Enhanced Biological Phosphorus Removal Plants Albertsen, Mads; McIlroy, Simon J.; Stokholm-Bjerregaard, Mikkel Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01033	journal	July 2016
Mining traits for the enrichment and isolation of not-yet-cultured populations Zhang, An-Ni; Mao, Yanping; Wang, Yubo Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0708-4	journal	June 2019
Resolving the individual contribution of key microbial populations to enhanced biological phosphorus removal with Raman–FISH Fernando, Eustace Y.; McIlroy, Simon Jon; Nierychlo, Marta The ISME Journal, Vol. 13, Issue 8 https://doi.org/10.1038/s41396-019-0399-7	journal	March 2019
The environment selects: Modeling energy allocation in microbial communities under dynamic environments da Silva, Leonor Guedes; Tomás-Martínez, Sergio; van Loosdrecht, Mark C. M. https://doi.org/10.1101/689174	preprint	July 2019
Integrated omics analyses reveal differential gene expression and potential for cooperation between denitrifying polyphosphate and glycogen accumulating organisms Wang, Yubo; Gao, Han; Wells, George Environmental Microbiology, Vol. 23, Issue 6 https://doi.org/10.1111/1462-2920.15486	journal	May 2021
Bacterial microcompartment-directed polyphosphate kinase promotes stable polyphosphate accumulation in E. coli Liang, Mingzhi; Frank, Stefanie; Lünsdorf, Heinrich Biotechnology Journal, Vol. 12, Issue 3 https://doi.org/10.1002/biot.201600415	journal	February 2017
Compositional analysis of archaeal communities in high and low microbial abundance sponges in the Misool coral reef system, Indonesia Polónia, Ana Rita Moura; Cleary, Daniel Francis Richard; Coelho, Francisco José Riso da Costa Marine Biology Research, Vol. 14, Issue 6 https://doi.org/10.1080/17451000.2018.1498977	journal	July 2018
The proteome of Tetrasphaera elongata is adapted to changing conditions in wastewater treatment plants Herbst, Florian-Alexander; Dueholm, Morten S.; Wimmer, Reinhard Proteomes https://doi.org/10.1101/513143	posted_content	April 2019

Similar Records

Integrated Omic Analyses Provide Evidence that a “ Candidatus Accumulibacter phosphatis” Strain Performs Denitrification under Microaerobic Conditions

Journal Article · Tue Feb 26 00:00:00 EST 2019 · mSystems · OSTI ID:1346927

Camejo, Pamela Y.; Oyserman, Ben O.; McMahon, Katherine D.; +2 more

Metabolic Differentiation of Co-occurring Accumulibacter Clades Revealed through Genome-Resolved Metatranscriptomics

Journal Article · Tue Jul 06 00:00:00 EDT 2021 · mSystems · OSTI ID:1346927

McDaniel, Elizabeth A.; Moya-Flores, Francisco; Keene Beach, Natalie; +6 more

Community proteogenomics highlights microbial strain-variant protein expression within activated sludge performing enhanced biological phosphorus removal.

Journal Article · Tue Jan 01 00:00:00 EST 2008 · The ISME Journal: Multidisciplinary Journal of Microbial Ecology · OSTI ID:1346927

Wilmes, P; Andersson, Anders F.; Lefsrud, Mark G; +6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
54 ENVIRONMENTAL SCIENCES

Title: Metatranscriptomic insights on gene expression and regulatory controls in Candidatus Accumulibacter phosphatis

Citation Formats

References (64)

Cited By (17)

Similar Records

Related Subjects