Involvement in Denitrification is Beneficial to the Biofilm Lifestyle of Comamonas testosteroni: A Mechanistic Study and Its Environmental Implications.
Comamonas is one of the most abundant microorganisms in biofilm communities driving wastewater treatment. Little has been known about the role of this group of organisms and their biofilm mode of life. In this study, using Comamonas testosteroni as a model organism, we demonstrated the involvement of Comamonas biofilms in denitrification under bulk aerobic conditions and elucidated the influence of nitrate respiration on its biofilm lifestyle. Our results showed that C. testosteroni could use nitrate as the sole electron acceptor for anaerobic growth. Under bulk aerobic condition, biofilms of C. testosteroni were capable of reducing nitrate, and intriguingly, nitrate reduction significantly enhanced viability of the biofilm-cells and reduced cell detachment from the biofilms. Nitrate respiration was further shown to play an essential role in maintaining high cell viability in the biofilms. RNA-seq analysis, quantitative polymerase chain reaction, and liquid chromatography-mass spectrometry revealed a higher level of bis(3'-5')-cyclic dimeric guanosine monophosphate (c-di-GMP) in cells respiring on nitrate than those grown aerobically (1.3 × 10(-4) fmol/cell vs 7.9 × 10(-6) fmol/cell; P < 0.01). C-di-GMP is one universal signaling molecule that regulates the biofilm mode of life, and a higher c-di-GMP concentration reduces cell detachment from biofilms. Taking these factors together, this study reveals that nitrate reduction occurs in mature biofilms of C. testosteroni under bulk aerobic conditions, and the respiratory reduction of nitrate is beneficial to the biofilm lifestyle by providing more metabolic energy to maintain high viability and a higher level of c-di-GMP to reduce cell detachment.
School of Civil and Environmental Engineering, Nanyang Technological University , 50 Nanyang Avenue, Singapore 639798.|Singapore Centre on Environmental Life Sciences Engineering, Nanyang Technological University , 60 Nanyang Drive, Singapore 637551.
Yichao
Y
Wu
School of Civil and Environmental Engineering, Nanyang Technological University , 50 Nanyang Avenue, Singapore 639798.|Singapore Centre on Environmental Life Sciences Engineering, Nanyang Technological University , 60 Nanyang Drive, Singapore 637551.
Sudha
S
Shukal
School of Civil and Environmental Engineering, Nanyang Technological University , 50 Nanyang Avenue, Singapore 639798.|Singapore Centre on Environmental Life Sciences Engineering, Nanyang Technological University , 60 Nanyang Drive, Singapore 637551.
Manisha
M
Mukherjee
School of Civil and Environmental Engineering, Nanyang Technological University , 50 Nanyang Avenue, Singapore 639798.|Singapore Centre on Environmental Life Sciences Engineering, Nanyang Technological University , 60 Nanyang Drive, Singapore 637551.
Bin
B
Cao
D000332:Aerobiosis; D018441:Biofilms / Q000254:growth & development; D020604:Comamonas testosteroni / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D006152:Cyclic GMP / Q000031:analogs & derivatives / Q000378:metabolism; D058440:Denitrification; D015964:Gene Expression Regulation, Bacterial; D009566:Nitrates / Q000378:metabolism; D016133:Polymerase Chain Reaction; D017423:Sequence Analysis, RNA; D062065:Wastewater / Q000382:microbiology*
D006152:Cyclic GMP; D009566:Nitrates; D062065:Wastewater; C062025:bis(3',5')-cyclic diguanylic acid