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 o...

Full description

Bibliographic Details
Main Authors: Wu, Yichao, Shukal, Sudha, Mukherjee, Manisha, Cao, Bin
Other Authors: School of Civil and Environmental Engineering
Format: Journal Article
Language:English
Published: 2015
Subjects:
Online Access:https://hdl.handle.net/10356/80969
http://hdl.handle.net/10220/38969
_version_ 1826115189991276544
author Wu, Yichao
Shukal, Sudha
Mukherjee, Manisha
Cao, Bin
author2 School of Civil and Environmental Engineering
author_facet School of Civil and Environmental Engineering
Wu, Yichao
Shukal, Sudha
Mukherjee, Manisha
Cao, Bin
author_sort Wu, Yichao
collection NTU
description 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.
first_indexed 2024-10-01T03:51:10Z
format Journal Article
id ntu-10356/80969
institution Nanyang Technological University
language English
last_indexed 2024-10-01T03:51:10Z
publishDate 2015
record_format dspace
spelling ntu-10356/809692020-09-21T11:32:50Z Involvement in Denitrification is Beneficial to the Biofilm Lifestyle of Comamonas testosteroni: A Mechanistic Study and Its Environmental Implications Wu, Yichao Shukal, Sudha Mukherjee, Manisha Cao, Bin School of Civil and Environmental Engineering Singapore Centre for Environmental Life Sciences Engineering DRNTU::Engineering::Environmental engineering::Water treatment 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. NRF (Natl Research Foundation, S’pore) MOE (Min. of Education, S’pore) Accepted version 2015-12-04T08:23:53Z 2019-12-06T14:18:34Z 2015-12-04T08:23:53Z 2019-12-06T14:18:34Z 2015 Journal Article Wu, Y., Shukal, S., Mukherjee, M.,& Cao, B. (2015). Involvement in Denitrification is Beneficial to the Biofilm Lifestyle of Comamonas testosteroni: A Mechanistic Study and Its Environmental Implications. Environmental Science & Technology, 49(19), 11551-11559. 0013-936X https://hdl.handle.net/10356/80969 http://hdl.handle.net/10220/38969 10.1021/acs.est.5b03381 en Environmental Science & Technology © 2015 American Chemical Society. This is the author created version of a work that has been peer reviewed and accepted for publication by Environmental Science & Technology, American Chemical Society. It incorporates referee’s comments but changes resulting from the publishing process, such as copyediting, structural formatting, may not be reflected in this document. The published version is available at: [http://dx.doi.org/10.1021/acs.est.5b03381]. 26 p. application/pdf
spellingShingle DRNTU::Engineering::Environmental engineering::Water treatment
Wu, Yichao
Shukal, Sudha
Mukherjee, Manisha
Cao, Bin
Involvement in Denitrification is Beneficial to the Biofilm Lifestyle of Comamonas testosteroni: A Mechanistic Study and Its Environmental Implications
title Involvement in Denitrification is Beneficial to the Biofilm Lifestyle of Comamonas testosteroni: A Mechanistic Study and Its Environmental Implications
title_full Involvement in Denitrification is Beneficial to the Biofilm Lifestyle of Comamonas testosteroni: A Mechanistic Study and Its Environmental Implications
title_fullStr Involvement in Denitrification is Beneficial to the Biofilm Lifestyle of Comamonas testosteroni: A Mechanistic Study and Its Environmental Implications
title_full_unstemmed Involvement in Denitrification is Beneficial to the Biofilm Lifestyle of Comamonas testosteroni: A Mechanistic Study and Its Environmental Implications
title_short Involvement in Denitrification is Beneficial to the Biofilm Lifestyle of Comamonas testosteroni: A Mechanistic Study and Its Environmental Implications
title_sort involvement in denitrification is beneficial to the biofilm lifestyle of comamonas testosteroni a mechanistic study and its environmental implications
topic DRNTU::Engineering::Environmental engineering::Water treatment
url https://hdl.handle.net/10356/80969
http://hdl.handle.net/10220/38969
work_keys_str_mv AT wuyichao involvementindenitrificationisbeneficialtothebiofilmlifestyleofcomamonastestosteroniamechanisticstudyanditsenvironmentalimplications
AT shukalsudha involvementindenitrificationisbeneficialtothebiofilmlifestyleofcomamonastestosteroniamechanisticstudyanditsenvironmentalimplications
AT mukherjeemanisha involvementindenitrificationisbeneficialtothebiofilmlifestyleofcomamonastestosteroniamechanisticstudyanditsenvironmentalimplications
AT caobin involvementindenitrificationisbeneficialtothebiofilmlifestyleofcomamonastestosteroniamechanisticstudyanditsenvironmentalimplications