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

Journal Article · Tue Jul 23 00:00:00 EDT 2019 · Algal Research

DOI:https://doi.org/10.1016/j.algal.2019.101580· OSTI ID:1544629

Bohutskyi, Pavlo  ^[1]; McClure, Ryan S. ^[1]; Hill, Eric A. ^[1]; Nelson, William C.  ^[1]; Chrisler, William B. ^[1]; Nuñez, Jamie R. ^[1]; Renslow, Ryan S.  ^[1]; Charania, Moiz A. ^[1]; Lindemann, Stephen R. ^[2]; Beliaev, Alexander S.  ^[3]

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

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.

• Research Organization: Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
• Sponsoring Organization: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Energy Efficiency and Renewable Energy (EERE), Transportation Office. Bioenergy Technologies Office
• Grant/Contract Number: AC05-76RL01830
• OSTI ID: 1544629
• Alternate ID(s): OSTI ID: 1694273
• Report Number(s): PNNL-SA-136164
• Journal Information: Algal Research, Vol. 42, Issue C; ISSN 2211-9264
• Publisher: Elsevier
• Country of Publication: United States
• Language: English

Related Subjects

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