Genomic and in Situ Analyses Reveal the Micropruina spp. as Abundant Fermentative Glycogen Accumulating Organisms in Enhanced Biological Phosphorus Removal Systems

Simon Jon McIlroy, Cristobal Andres Onetto Carvallo, Bianca McIlroy, Florian-Alexander Herbst, Morten Simonsen Dueholm, Rasmus Hansen Kirkegaard, Eustace Yrosh Fernando Warnakulasuriya, Søren Michael Karst, Marta Nierychlo, Jannie Munk Kristensen, Kathryn L. Eales, Paul R. Grbin, Reinhard Wimmer, Per Halkjær Nielsen

Eksport af forskningsdata: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

8 Citationer (Scopus)
165 Downloads (Pure)

Resumé

Enhanced biological phosphorus removal (EBPR) involves the cycling of biomass through carbon-rich (feast) and carbon-deficient (famine) conditions, promoting the activity of polyphosphate accumulating organisms (PAOs). However, several alternate metabolic strategies, without polyphosphate storage, are possessed by other organisms, which can compete with the PAO for carbon at the potential expense of EBPR efficiency. The most studied are the glycogen accumulating organisms (GAOs), which utilize aerobically stored glycogen to energize anaerobic substrate uptake and storage. In full-scale systems the Micropruina spp. are among the most abundant of the proposed GAO, yet little is known about their ecophysiology. In the current study, genomic and metabolomic studies were performed on Micropruina glycogenica str. Lg2 T and compared to the in situ physiology of members of the genus in EBPR plants using state-of-the-art single cell techniques. The Micropruina spp. were observed to take up carbon, including sugars and amino acids, under anaerobic conditions, which were partly fermented to lactic acid, acetate, propionate, and ethanol, and partly stored as glycogen for potential aerobic use. Fermentation was not directly demonstrated for the abundant members of the genus in situ, but was strongly supported by the confirmation of anaerobic uptake of carbon and glycogen storage in the absence of detectable polyhydroxyalkanoates or polyphosphate reserves. This physiology is markedly different from the classical GAO model. The amount of carbon stored by fermentative organisms has potentially important implications for phosphorus removal - as they compete for substrates with the Tetrasphaera PAO and stored carbon is not made available to the "Candidatus Accumulibacter" PAO under anaerobic conditions. This study shows that the current models of the competition between PAO and GAO are too simplistic and may need to be revised to take into account the impact of potential carbon storage by fermentative organisms.

OriginalsprogEngelsk
Artikelnummer1004
TidsskriftFrontiers in Microbiology
Vol/bind9
Antal sider12
ISSN1664-302X
DOI'er
PublikationsstatusUdgivet - 23 maj 2018

Fingerprint

Polyphosphates
Glycogen
Phosphorus
Carbon
Polyhydroxyalkanoates
Sugar Acids
Metabolomics
Propionates
Starvation
Biomass
Fermentation
Lactic Acid
Acetates
Ethanol
Amino Acids

Citer dette

@article{c187ea7407d0493881b76820dd5e9a8c,
title = "Genomic and in Situ Analyses Reveal the Micropruina spp. as Abundant Fermentative Glycogen Accumulating Organisms in Enhanced Biological Phosphorus Removal Systems",
abstract = "Enhanced biological phosphorus removal (EBPR) involves the cycling of biomass through carbon-rich (feast) and carbon-deficient (famine) conditions, promoting the activity of polyphosphate accumulating organisms (PAOs). However, several alternate metabolic strategies, without polyphosphate storage, are possessed by other organisms, which can compete with the PAO for carbon at the potential expense of EBPR efficiency. The most studied are the glycogen accumulating organisms (GAOs), which utilize aerobically stored glycogen to energize anaerobic substrate uptake and storage. In full-scale systems the Micropruina spp. are among the most abundant of the proposed GAO, yet little is known about their ecophysiology. In the current study, genomic and metabolomic studies were performed on Micropruina glycogenica str. Lg2 T and compared to the in situ physiology of members of the genus in EBPR plants using state-of-the-art single cell techniques. The Micropruina spp. were observed to take up carbon, including sugars and amino acids, under anaerobic conditions, which were partly fermented to lactic acid, acetate, propionate, and ethanol, and partly stored as glycogen for potential aerobic use. Fermentation was not directly demonstrated for the abundant members of the genus in situ, but was strongly supported by the confirmation of anaerobic uptake of carbon and glycogen storage in the absence of detectable polyhydroxyalkanoates or polyphosphate reserves. This physiology is markedly different from the classical GAO model. The amount of carbon stored by fermentative organisms has potentially important implications for phosphorus removal - as they compete for substrates with the Tetrasphaera PAO and stored carbon is not made available to the {"}Candidatus Accumulibacter{"} PAO under anaerobic conditions. This study shows that the current models of the competition between PAO and GAO are too simplistic and may need to be revised to take into account the impact of potential carbon storage by fermentative organisms.",
author = "McIlroy, {Simon Jon} and Carvallo, {Cristobal Andres Onetto} and Bianca McIlroy and Florian-Alexander Herbst and Dueholm, {Morten Simonsen} and Kirkegaard, {Rasmus Hansen} and Warnakulasuriya, {Eustace Yrosh Fernando} and Karst, {S{\o}ren Michael} and Marta Nierychlo and Kristensen, {Jannie Munk} and Eales, {Kathryn L.} and Grbin, {Paul R.} and Reinhard Wimmer and Nielsen, {Per Halkj{\ae}r}",
year = "2018",
month = "5",
day = "23",
doi = "10.3389/fmicb.2018.01004",
language = "English",
volume = "9",
journal = "Frontiers in Microbiology",
issn = "1664-302X",
publisher = "Frontiers Media S.A.",

}

Genomic and in Situ Analyses Reveal the Micropruina spp. as Abundant Fermentative Glycogen Accumulating Organisms in Enhanced Biological Phosphorus Removal Systems. / McIlroy, Simon Jon; Carvallo, Cristobal Andres Onetto; McIlroy, Bianca; Herbst, Florian-Alexander; Dueholm, Morten Simonsen; Kirkegaard, Rasmus Hansen; Warnakulasuriya, Eustace Yrosh Fernando; Karst, Søren Michael; Nierychlo, Marta; Kristensen, Jannie Munk; Eales, Kathryn L.; Grbin, Paul R.; Wimmer, Reinhard; Nielsen, Per Halkjær.

i: Frontiers in Microbiology, Bind 9, 1004, 23.05.2018.

Eksport af forskningsdata: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

TY - JOUR

T1 - Genomic and in Situ Analyses Reveal the Micropruina spp. as Abundant Fermentative Glycogen Accumulating Organisms in Enhanced Biological Phosphorus Removal Systems

AU - McIlroy, Simon Jon

AU - Carvallo, Cristobal Andres Onetto

AU - McIlroy, Bianca

AU - Herbst, Florian-Alexander

AU - Dueholm, Morten Simonsen

AU - Kirkegaard, Rasmus Hansen

AU - Warnakulasuriya, Eustace Yrosh Fernando

AU - Karst, Søren Michael

AU - Nierychlo, Marta

AU - Kristensen, Jannie Munk

AU - Eales, Kathryn L.

AU - Grbin, Paul R.

AU - Wimmer, Reinhard

AU - Nielsen, Per Halkjær

PY - 2018/5/23

Y1 - 2018/5/23

N2 - Enhanced biological phosphorus removal (EBPR) involves the cycling of biomass through carbon-rich (feast) and carbon-deficient (famine) conditions, promoting the activity of polyphosphate accumulating organisms (PAOs). However, several alternate metabolic strategies, without polyphosphate storage, are possessed by other organisms, which can compete with the PAO for carbon at the potential expense of EBPR efficiency. The most studied are the glycogen accumulating organisms (GAOs), which utilize aerobically stored glycogen to energize anaerobic substrate uptake and storage. In full-scale systems the Micropruina spp. are among the most abundant of the proposed GAO, yet little is known about their ecophysiology. In the current study, genomic and metabolomic studies were performed on Micropruina glycogenica str. Lg2 T and compared to the in situ physiology of members of the genus in EBPR plants using state-of-the-art single cell techniques. The Micropruina spp. were observed to take up carbon, including sugars and amino acids, under anaerobic conditions, which were partly fermented to lactic acid, acetate, propionate, and ethanol, and partly stored as glycogen for potential aerobic use. Fermentation was not directly demonstrated for the abundant members of the genus in situ, but was strongly supported by the confirmation of anaerobic uptake of carbon and glycogen storage in the absence of detectable polyhydroxyalkanoates or polyphosphate reserves. This physiology is markedly different from the classical GAO model. The amount of carbon stored by fermentative organisms has potentially important implications for phosphorus removal - as they compete for substrates with the Tetrasphaera PAO and stored carbon is not made available to the "Candidatus Accumulibacter" PAO under anaerobic conditions. This study shows that the current models of the competition between PAO and GAO are too simplistic and may need to be revised to take into account the impact of potential carbon storage by fermentative organisms.

AB - Enhanced biological phosphorus removal (EBPR) involves the cycling of biomass through carbon-rich (feast) and carbon-deficient (famine) conditions, promoting the activity of polyphosphate accumulating organisms (PAOs). However, several alternate metabolic strategies, without polyphosphate storage, are possessed by other organisms, which can compete with the PAO for carbon at the potential expense of EBPR efficiency. The most studied are the glycogen accumulating organisms (GAOs), which utilize aerobically stored glycogen to energize anaerobic substrate uptake and storage. In full-scale systems the Micropruina spp. are among the most abundant of the proposed GAO, yet little is known about their ecophysiology. In the current study, genomic and metabolomic studies were performed on Micropruina glycogenica str. Lg2 T and compared to the in situ physiology of members of the genus in EBPR plants using state-of-the-art single cell techniques. The Micropruina spp. were observed to take up carbon, including sugars and amino acids, under anaerobic conditions, which were partly fermented to lactic acid, acetate, propionate, and ethanol, and partly stored as glycogen for potential aerobic use. Fermentation was not directly demonstrated for the abundant members of the genus in situ, but was strongly supported by the confirmation of anaerobic uptake of carbon and glycogen storage in the absence of detectable polyhydroxyalkanoates or polyphosphate reserves. This physiology is markedly different from the classical GAO model. The amount of carbon stored by fermentative organisms has potentially important implications for phosphorus removal - as they compete for substrates with the Tetrasphaera PAO and stored carbon is not made available to the "Candidatus Accumulibacter" PAO under anaerobic conditions. This study shows that the current models of the competition between PAO and GAO are too simplistic and may need to be revised to take into account the impact of potential carbon storage by fermentative organisms.

U2 - 10.3389/fmicb.2018.01004

DO - 10.3389/fmicb.2018.01004

M3 - Journal article

VL - 9

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

M1 - 1004

ER -