Transcriptomic and proteomic analyses of Desulfovibrio vulgaris biofilms: Carbon and energy flow contribute to the distinct biofilm growth state

Clark, Melinda E.; He, Zhili; Redding, Alyssa M.; Joachimiak, Marcin P.; Keasling, Jay D.; Zhou, Jizhong Z.; Arkin, Adam P.; Mukhopadhyay, Aindrila; Fields, Matthew W.

doi:10.1186/1471-2164-13-138

Transcriptomic and proteomic analyses of Desulfovibrio vulgaris biofilms: Carbon and energy flow contribute to the distinct biofilm growth state

Journal Article · Sun Jan 01 00:00:00 EST 2012 · BMC Genomics

DOI:https://doi.org/10.1186/1471-2164-13-138· OSTI ID:1626414

Clark, Melinda E. ^[1]; He, Zhili ^[2]; Redding, Alyssa M. ^[3]; Joachimiak, Marcin P. ^[4]; Keasling, Jay D. ^[5]; Zhou, Jizhong Z. ^[2]; Arkin, Adam P. ^[6]; Mukhopadhyay, Aindrila ^[4]; Fields, Matthew W. ^[7]

Miami Univ., Oxford, OH (United States). Dept. of Microbiology; Montana State Univ., Bozeman, MT (United States). Center for Biofilm Engineering; DOE/OSTI
Univ. of Oklahoma, Norman, OK (United States). Inst. for Environmental Genomics; Environmental Networks Integrated with Molecular Assemblies (http://enigma.lbl.gov/), Bozeman, MT (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division; Environmental Networks Integrated with Molecular Assemblies (http://enigma.lbl.gov/), Bozeman, MT (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division; Univ. of California, Berkeley, CA (United States). Dept. of Chemical and Biomolecular Engineering; Univ. of California, Berkeley, CA (United States). Dept. of Bioengineering; Environmental Networks Integrated with Molecular Assemblies (http://enigma.lbl.gov/), Bozeman, MT (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division; Univ. of California, Berkeley, CA (United States). Dept. of Bioengineering; Environmental Networks Integrated with Molecular Assemblies (http://enigma.lbl.gov/), Bozeman, MT (United States)
Montana State Univ., Bozeman, MT (United States). Center for Biofilm Engineering; Environmental Networks Integrated with Molecular Assemblies (http://enigma.lbl.gov/), Bozeman, MT (United States)

Background: Desulfovibrio vulgaris Hildenborough is a sulfate-reducing bacterium (SRB) that is intensively studied in the context of metal corrosion and heavy-metal bioremediation, and SRB populations are commonly observed in pipe and subsurface environments as surface-associated populations. In order to elucidate physiological changes associated with biofilm growth at both the transcript and protein level, transcriptomic and proteomic analyses were done on mature biofilm cells and compared to both batch and reactor planktonic populations. The biofilms were cultivated with lactate and sulfate in a continuously fed biofilm reactor, and compared to both batch and reactor planktonic populations. Results: The functional genomic analysis demonstrated that biofilm cells were different compared to planktonic cells, and the majority of altered abundances for genes and proteins were annotated as hypothetical (unknown function), energy conservation, amino acid metabolism, and signal transduction. Genes and proteins that showed similar trends in detected levels were particularly involved in energy conservation such as increases in an annotated ech hydrogenase, formate dehydrogenase, pyruvate:ferredoxin oxidoreductase, and rnf oxidoreductase, and the biofilm cells had elevated formate dehydrogenase activity. Several other hydrogenases and formate dehydrogenases also showed an increased protein level, while decreased transcript and protein levels were observed for putative coo hydrogenase as well as a lactate permease and hyp hydrogenases for biofilm cells. Genes annotated for amino acid synthesis and nitrogen utilization were also predominant changers within the biofilm state. Ribosomal transcripts and proteins were notably decreased within the biofilm cells compared to exponential-phase cells but were not as low as levels observed in planktonic, stationary-phase cells. Several putative, extracellular proteins (DVU1012, 1545) were also detected in the extracellular fraction from biofilm cells. Conclusions: Even though both the planktonic and biofilm cells were oxidizing lactate and reducing sulfate, the biofilm cells were physiologically distinct compared to planktonic growth states due to altered abundances of genes/proteins involved in carbon/energy flow and extracellular structures. In addition, average expression values for multiple rRNA transcripts and respiratory activity measurements indicated that biofilm cells were metabolically more similar to exponential-phase cells although biofilm cells are structured differently. The characterization of physiological advantages and constraints of the biofilm growth state for sulfate-reducing bacteria will provide insight into bioremediation applications as well as microbially-induced metal corrosion.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1626414

Journal Information:: BMC Genomics, Journal Name: BMC Genomics Journal Issue: 1 Vol. 13; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Rapid selective sweep of pre-existing polymorphisms and slow fixation of new mutations in experimental evolution of Desulfovibrio vulgaris Zhou, Aifen; Hillesland, Kristina L.; He, Zhili The ISME Journal, Vol. 9, Issue 11 https://doi.org/10.1038/ismej.2015.45	journal	April 2015
Molecular regulation of adhesion and biofilm formation in high and low biofilm producers of Bacillus licheniformis using RNA-Seq Sadiq, Faizan Ahmed; Flint, Steve; Sakandar, Hafiz Arbab Biofouling, Vol. 35, Issue 2 https://doi.org/10.1080/08927014.2019.1575960	journal	February 2019
Bulk phase resource ratio alters carbon steel corrosion rates and endogenously produced extracellular electron transfer mediators in a sulfate-reducing biofilm Krantz, Gregory P.; Lucas, Kilean; Wunderlich, Erica L. - Biofouling, Vol. 35, Issue 6 https://doi.org/10.1080/08927014.2019.1646731	journal	July 2019
Impact of hydrologic boundaries on microbial planktonic and biofilm communities in shallow terrestrial subsurface environments Smith, H. J.; Zelaya, A. J.; De León, K. B. FEMS Microbiology Ecology, Vol. 94, Issue 12 https://doi.org/10.1093/femsec/fiy191	journal	September 2018
σ ₅₄ ‐Dependent regulator DVU2956 switches Desulfovibrio vulgaris from biofilm formation to planktonic growth and regulates hydrogen sulfide production Zhu, Lei; Gong, Ting; Wood, Thammajun L. Environmental Microbiology, Vol. 21, Issue 10 https://doi.org/10.1111/1462-2920.14679	journal	May 2019
Microbial Surface Colonization and Biofilm Development in Marine Environments Dang, Hongyue; Lovell, Charles R. Microbiology and Molecular Biology Reviews, Vol. 80, Issue 1 https://doi.org/10.1128/mmbr.00037-15	journal	December 2015
Potential role of multiple carbon fixation pathways during lipid accumulation in Phaeodactylum tricornutum Valenzuela, Jacob; Mazurie, Aurelien; Carlson, Ross P. Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-40	journal	January 2012
Bulk phase resource ratio alters carbon steel corrosion rates and endogenously produced extracellular electron transfer mediators in a sulfate-reducing biofilm Krantz, Gregory P.; Lucas, Kilean; Wunderlich, Erica L. - Taylor & Francis https://doi.org/10.6084/m9.figshare.9505367	text	January 2019
Bulk phase resource ratio alters carbon steel corrosion rates and endogenously produced extracellular electron transfer mediators in a sulfate-reducing biofilm Krantz, Gregory P.; Lucas, Kilean; Wunderlich, Erica L. - Taylor & Francis https://doi.org/10.6084/m9.figshare.9505367.v1	text	January 2019

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