Metabolic effects of vitamin B12 on physiology, stress resistance, growth rate and biomass productivity of Cyanobacterium stanieri planktonic and biofilm cultures

Bohutskyi, Pavlo; McClure, Ryan S.; Hill, Eric A.; Nelson, William C.; Chrisler, William B.; Nuñez, Jamie R.; Renslow, Ryan S.; Charania, Moiz A.; Lindemann, Stephen R.; Beliaev, Alexander S.

doi:10.1016/j.algal.2019.101580

Title: Metabolic effects of vitamin B12 on physiology, stress resistance, growth rate and biomass productivity of Cyanobacterium stanieri planktonic and biofilm cultures

Abstract

Although synthesized only by bacteria and archaea, cobalamin (vitamin B₁₂) is essential for virtually all living cells. One major function is its role in methionine synthesis, as a co-factor for the B₁₂-dependent methionine synthase MetH. However, a large number of microbes avoid requirements for B₁₂ by encoding cobalamin-independent enzymes, such as the B₁₂-independent methionine synthase MetE. Interestingly, many such microbes retain transporters for exogenous B₁₂, produced by neighboring microbes. We hypothesize that selection for retention of B₁₂ transport suggests preservation of unrevealed but critical roles for cobalamin in photoautotroph fitness. As such, to identify the impacts of B₁₂ on photoautotrophic metabolism, we studied the physiological and transcriptional adaptation of Cyanobacterium stanieri HL-69 to varying irradiance and oxidative stress in the presence and absence of B₁₂. The metabolic flexibility of C. stanieri, which possesses both MetH and MetE, allows comparative analysis of cobalamin impacts on its global metabolism. As anticipated, B₁₂ availability governed transcription of cobalamin transporter btuB, metH and a number of genes involved in the methionine-folate cycle. Surprisingly, however, B₁₂ impacted the cell integrity, growth rate and biomass productivity of C. stanieri under conditions of likely oxidative stress due to biofilm growth or under high partial pressures of O₂.more »« less

Authors:

^[1]; McClure, Ryan S. ^[1]; Hill, Eric A. ^[1];

^[1]; Chrisler, William B. ^[1]; Nuñez, Jamie R. ^[1];

^[1]; Charania, Moiz A. ^[1]; Lindemann, Stephen R. ^[2];

^[3]

Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Purdue Univ., West Lafayette, IN (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Queensland Univ. of Technology, Brisbane (Australia)

Publication Date:: Tue Jul 23 00:00:00 EDT 2019

Research Org.:: Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Energy Efficiency and Renewable Energy (EERE), Transportation Office. Bioenergy Technologies Office

OSTI Identifier:: 1544629

Alternate Identifier(s):: OSTI ID: 1694273

Report Number(s):: PNNL-SA-136164
Journal ID: ISSN 2211-9264

Grant/Contract Number:: AC05-76RL01830

Resource Type:: Accepted Manuscript

Journal Name:: Algal Research

Additional Journal Information:: Journal Volume: 42; Journal Issue: C; Journal ID: ISSN 2211-9264

Publisher:: Elsevier

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Vitamin B12; Biofilm organization; High irradiance and oxidative stress; Transcriptional adaptation; Improved growth rate and productivity; Oxidative stress resistance

Citation Formats


                    Bohutskyi, Pavlo, McClure, Ryan S., Hill, Eric A., Nelson, William C., Chrisler, William B., Nuñez, Jamie R., Renslow, Ryan S., Charania, Moiz A., Lindemann, Stephen R., and Beliaev, Alexander S. Metabolic effects of vitamin B12 on physiology, stress resistance, growth rate and biomass productivity of Cyanobacterium stanieri planktonic and biofilm cultures.  United States: N. p., 2019. 
Web.  doi:10.1016/j.algal.2019.101580.

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                    Bohutskyi, Pavlo, McClure, Ryan S., Hill, Eric A., Nelson, William C., Chrisler, William B., Nuñez, Jamie R., Renslow, Ryan S., Charania, Moiz A., Lindemann, Stephen R., & Beliaev, Alexander S. Metabolic effects of vitamin B12 on physiology, stress resistance, growth rate and biomass productivity of Cyanobacterium stanieri planktonic and biofilm cultures.  United States.  https://doi.org/10.1016/j.algal.2019.101580

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                    Bohutskyi, Pavlo, McClure, Ryan S., Hill, Eric A., Nelson, William C., Chrisler, William B., Nuñez, Jamie R., Renslow, Ryan S., Charania, Moiz A., Lindemann, Stephen R., and Beliaev, Alexander S. Tue .  
"Metabolic effects of vitamin B12 on physiology, stress resistance, growth rate and biomass productivity of Cyanobacterium stanieri planktonic and biofilm cultures".  United States.  https://doi.org/10.1016/j.algal.2019.101580.  https://www.osti.gov/servlets/purl/1544629.

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@article{osti_1544629,

  title        = {Metabolic effects of vitamin B12 on physiology, stress resistance, growth rate and biomass productivity of Cyanobacterium stanieri planktonic and biofilm cultures},

  author       = {Bohutskyi, Pavlo and McClure, Ryan S. and Hill, Eric A. and Nelson, William C. and Chrisler, William B. and Nuñez, Jamie R. and Renslow, Ryan S. and Charania, Moiz A. and Lindemann, Stephen R. and Beliaev, Alexander S.},

  abstractNote = {Although synthesized only by bacteria and archaea, cobalamin (vitamin B12) is essential for virtually all living cells. One major function is its role in methionine synthesis, as a co-factor for the B12-dependent methionine synthase MetH. However, a large number of microbes avoid requirements for B12 by encoding cobalamin-independent enzymes, such as the B12-independent methionine synthase MetE. Interestingly, many such microbes retain transporters for exogenous B12, produced by neighboring microbes. We hypothesize that selection for retention of B12 transport suggests preservation of unrevealed but critical roles for cobalamin in photoautotroph fitness. As such, to identify the impacts of B12 on photoautotrophic metabolism, we studied the physiological and transcriptional adaptation of Cyanobacterium stanieri HL-69 to varying irradiance and oxidative stress in the presence and absence of B12. The metabolic flexibility of C. stanieri, which possesses both MetH and MetE, allows comparative analysis of cobalamin impacts on its global metabolism. As anticipated, B12 availability governed transcription of cobalamin transporter btuB, metH and a number of genes involved in the methionine-folate cycle. Surprisingly, however, B12 impacted the cell integrity, growth rate and biomass productivity of C. stanieri under conditions of likely oxidative stress due to biofilm growth or under high partial pressures of O2. Furthermore, C. stanieri response to B12 globally rewired cellular metabolic networks, including nitrogen metabolism, energy metabolism, redox homeostasis and oxidative stress response. These findings demonstrate previously-unappreciated roles for B12 metabolism beyond methionine synthesis and reveal how interactions with cobalamin-producing heterotrophs may affect phytoplankton function and dynamics in natural microbial communities. Further comprehension and mastering of the natural oxidative stress resistance mechanisms modulated by cobalamin could be used for the design and implementation of more robust algal bioprocesses retaining high biomass productivities especially under stress conditions.},

  doi          = {10.1016/j.algal.2019.101580},

  journal      = {Algal Research},

  number       = C,

  volume       = 42,

  place        = {United States},

  year         = {Tue Jul 23 00:00:00 EDT 2019},

  month        = {Tue Jul 23 00:00:00 EDT 2019}

}

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https://doi.org/10.1016/j.algal.2019.101580

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Figures / Tables:

Figure 1: Quantitative assessment of C. stanieri biofilm morphology in the absence and presence of cobalamin. (A) Mean biofilm density assessed as mean non-background pixel intensity; (B) area of culture dish covered by biofilm; (C) biofilm heterogeneity assessed as heterogeneity in non-background pixel intensity; and (D) mean hue for non-backgroundmore »

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