The effect of bacterial community members on the proteome of the ammonia-oxidizing bacterium Nitrosomonas sp. Is79

Christopher J. Sedlacek; Susanne Nielsen; Kenneth D. Greis; Wendy D. Haffey; Niels Peter Revsbech; Tomislav Ticak; Hendrikus J. Laanbroek; Annette Bollmann

doi:10.1128/AEM.01171-16

The effect of bacterial community members on the proteome of the ammonia-oxidizing bacterium Nitrosomonas sp. Is79

Christopher J. Sedlacek, Susanne Nielsen, Kenneth D. Greis, Wendy D. Haffey, Niels Peter Revsbech, Tomislav Ticak, Hendrikus J. Laanbroek, Annette Bollmann

NIOO - Microbial Ecology (ME)

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Abstract

Microorganisms in the environment do not exist as the often-studied pure cultures but as members of complex microbial communities. Characterizing the interactions within microbial communities is essential to understand their function in both natural and engineered environments. In this study we investigated how the presence of a nitrite-oxidizing bacterium (NOB) and heterotrophic bacteria affect the growth and proteome of the chemolithoautotrophic ammonia-oxidizing bacterium (AOB) Nitrosomonas sp. Is79. We investigated Nitrosomonas sp. Is79, in co-culture with Nitrobacter winogradskyi, in co-cultures with selected heterotrophic bacteria and as a member of the nitrifying enrichment culture G5-7. In batch culture, N. winogradskyi and heterotrophic bacteria had positive effects on the growth of Nitrosomonas sp. Is79. An isobaric tag for a relative quantification (iTRAQ) LC MS/MS proteomics approach was used to investigate the effect of N. winogradskyi and the co-cultured heterotrophic bacteria from G5-7 on the proteome of Nitrosomonas sp. Is79. In co-culture with N. winogradskyi, several Nitrosomonas sp. Is79 oxidative stress response proteins changed in abundance with periplasmic proteins increasing and cytoplasmic proteins decreasing in abundance. In the presence of heterotrophic bacteria, the abundance of proteins directly related to the ammonia oxidation pathway increased, while the abundance of proteins related to amino acid synthesis and metabolism decreased. In summary, the proteome of Nitrosomonas sp. Is79 was differentially influenced by the presence of either N. winogradskyi or heterotrophic bacteria. Together, N. winogradskyi and heterotrophic bacteria reduced the oxidative stress for Nitrosomonas sp. Is79, which resulted in a more efficient metabolism.Importance Aerobic ammonia oxidizing microorganisms play an important role in the global nitrogen cycle, converting ammonia to nitrite. In their natural environment they coexist and interact with nitrite oxidizers, which convert nitrite to nitrate, and with heterotrophic microorganisms. The presence of nitrite oxidizers and heterotrophic bacteria has a positive influence on the growth of the ammonia oxidizers. Here we present a study investigating the effect of nitrite oxidizers and heterotrophic bacteria on the proteome of a selected ammonia oxidizer in a defined culture to elucidate how these two groups improve the performance of the ammonia oxidizer. The results show that the presence of nitrite oxidizers and heterotrophic bacteria reduced stress for the ammonia oxidizers and resulted in a more efficient energy generation. This study contributes to our understanding of microbe-microbe interactions, in particular between ammonia oxidizers and their neighboring microbial community.

Original language	English
Pages (from-to)	4776-4788
Journal	Applied and Environmental Microbiology
Volume	82
Issue number	15
Early online date	27 May 2016
DOIs	https://doi.org/10.1128/AEM.01171-16
Publication status	Published - 2016

Keywords

international

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http://aem.asm.org/content/early/2016/05/23/AEM.01171-16.abstract

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@article{b6279005bb544180b3525818398d20a1,

title = "The effect of bacterial community members on the proteome of the ammonia-oxidizing bacterium Nitrosomonas sp. Is79",

abstract = "Microorganisms in the environment do not exist as the often-studied pure cultures but as members of complex microbial communities. Characterizing the interactions within microbial communities is essential to understand their function in both natural and engineered environments. In this study we investigated how the presence of a nitrite-oxidizing bacterium (NOB) and heterotrophic bacteria affect the growth and proteome of the chemolithoautotrophic ammonia-oxidizing bacterium (AOB) Nitrosomonas sp. Is79. We investigated Nitrosomonas sp. Is79, in co-culture with Nitrobacter winogradskyi, in co-cultures with selected heterotrophic bacteria and as a member of the nitrifying enrichment culture G5-7. In batch culture, N. winogradskyi and heterotrophic bacteria had positive effects on the growth of Nitrosomonas sp. Is79. An isobaric tag for a relative quantification (iTRAQ) LC MS/MS proteomics approach was used to investigate the effect of N. winogradskyi and the co-cultured heterotrophic bacteria from G5-7 on the proteome of Nitrosomonas sp. Is79. In co-culture with N. winogradskyi, several Nitrosomonas sp. Is79 oxidative stress response proteins changed in abundance with periplasmic proteins increasing and cytoplasmic proteins decreasing in abundance. In the presence of heterotrophic bacteria, the abundance of proteins directly related to the ammonia oxidation pathway increased, while the abundance of proteins related to amino acid synthesis and metabolism decreased. In summary, the proteome of Nitrosomonas sp. Is79 was differentially influenced by the presence of either N. winogradskyi or heterotrophic bacteria. Together, N. winogradskyi and heterotrophic bacteria reduced the oxidative stress for Nitrosomonas sp. Is79, which resulted in a more efficient metabolism.Importance Aerobic ammonia oxidizing microorganisms play an important role in the global nitrogen cycle, converting ammonia to nitrite. In their natural environment they coexist and interact with nitrite oxidizers, which convert nitrite to nitrate, and with heterotrophic microorganisms. The presence of nitrite oxidizers and heterotrophic bacteria has a positive influence on the growth of the ammonia oxidizers. Here we present a study investigating the effect of nitrite oxidizers and heterotrophic bacteria on the proteome of a selected ammonia oxidizer in a defined culture to elucidate how these two groups improve the performance of the ammonia oxidizer. The results show that the presence of nitrite oxidizers and heterotrophic bacteria reduced stress for the ammonia oxidizers and resulted in a more efficient energy generation. This study contributes to our understanding of microbe-microbe interactions, in particular between ammonia oxidizers and their neighboring microbial community.",

keywords = "international",

author = "Sedlacek, {Christopher J.} and Susanne Nielsen and Greis, {Kenneth D.} and Haffey, {Wendy D.} and Revsbech, {Niels Peter} and Tomislav Ticak and Laanbroek, {Hendrikus J.} and Annette Bollmann",

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year = "2016",

doi = "10.1128/AEM.01171-16",

language = "English",

volume = "82",

pages = "4776--4788",

journal = "Applied and Environmental Microbiology",

issn = "0099-2240",

publisher = "American Society for Microbiology",

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TY - JOUR

T1 - The effect of bacterial community members on the proteome of the ammonia-oxidizing bacterium Nitrosomonas sp. Is79

AU - Sedlacek, Christopher J.

AU - Nielsen, Susanne

AU - Greis, Kenneth D.

AU - Haffey, Wendy D.

AU - Revsbech, Niels Peter

AU - Ticak, Tomislav

AU - Laanbroek, Hendrikus J.

AU - Bollmann, Annette

N1 - 6098, ME; Data Archiving: no data, dat with consortium

PY - 2016

Y1 - 2016

N2 - Microorganisms in the environment do not exist as the often-studied pure cultures but as members of complex microbial communities. Characterizing the interactions within microbial communities is essential to understand their function in both natural and engineered environments. In this study we investigated how the presence of a nitrite-oxidizing bacterium (NOB) and heterotrophic bacteria affect the growth and proteome of the chemolithoautotrophic ammonia-oxidizing bacterium (AOB) Nitrosomonas sp. Is79. We investigated Nitrosomonas sp. Is79, in co-culture with Nitrobacter winogradskyi, in co-cultures with selected heterotrophic bacteria and as a member of the nitrifying enrichment culture G5-7. In batch culture, N. winogradskyi and heterotrophic bacteria had positive effects on the growth of Nitrosomonas sp. Is79. An isobaric tag for a relative quantification (iTRAQ) LC MS/MS proteomics approach was used to investigate the effect of N. winogradskyi and the co-cultured heterotrophic bacteria from G5-7 on the proteome of Nitrosomonas sp. Is79. In co-culture with N. winogradskyi, several Nitrosomonas sp. Is79 oxidative stress response proteins changed in abundance with periplasmic proteins increasing and cytoplasmic proteins decreasing in abundance. In the presence of heterotrophic bacteria, the abundance of proteins directly related to the ammonia oxidation pathway increased, while the abundance of proteins related to amino acid synthesis and metabolism decreased. In summary, the proteome of Nitrosomonas sp. Is79 was differentially influenced by the presence of either N. winogradskyi or heterotrophic bacteria. Together, N. winogradskyi and heterotrophic bacteria reduced the oxidative stress for Nitrosomonas sp. Is79, which resulted in a more efficient metabolism.Importance Aerobic ammonia oxidizing microorganisms play an important role in the global nitrogen cycle, converting ammonia to nitrite. In their natural environment they coexist and interact with nitrite oxidizers, which convert nitrite to nitrate, and with heterotrophic microorganisms. The presence of nitrite oxidizers and heterotrophic bacteria has a positive influence on the growth of the ammonia oxidizers. Here we present a study investigating the effect of nitrite oxidizers and heterotrophic bacteria on the proteome of a selected ammonia oxidizer in a defined culture to elucidate how these two groups improve the performance of the ammonia oxidizer. The results show that the presence of nitrite oxidizers and heterotrophic bacteria reduced stress for the ammonia oxidizers and resulted in a more efficient energy generation. This study contributes to our understanding of microbe-microbe interactions, in particular between ammonia oxidizers and their neighboring microbial community.

AB - Microorganisms in the environment do not exist as the often-studied pure cultures but as members of complex microbial communities. Characterizing the interactions within microbial communities is essential to understand their function in both natural and engineered environments. In this study we investigated how the presence of a nitrite-oxidizing bacterium (NOB) and heterotrophic bacteria affect the growth and proteome of the chemolithoautotrophic ammonia-oxidizing bacterium (AOB) Nitrosomonas sp. Is79. We investigated Nitrosomonas sp. Is79, in co-culture with Nitrobacter winogradskyi, in co-cultures with selected heterotrophic bacteria and as a member of the nitrifying enrichment culture G5-7. In batch culture, N. winogradskyi and heterotrophic bacteria had positive effects on the growth of Nitrosomonas sp. Is79. An isobaric tag for a relative quantification (iTRAQ) LC MS/MS proteomics approach was used to investigate the effect of N. winogradskyi and the co-cultured heterotrophic bacteria from G5-7 on the proteome of Nitrosomonas sp. Is79. In co-culture with N. winogradskyi, several Nitrosomonas sp. Is79 oxidative stress response proteins changed in abundance with periplasmic proteins increasing and cytoplasmic proteins decreasing in abundance. In the presence of heterotrophic bacteria, the abundance of proteins directly related to the ammonia oxidation pathway increased, while the abundance of proteins related to amino acid synthesis and metabolism decreased. In summary, the proteome of Nitrosomonas sp. Is79 was differentially influenced by the presence of either N. winogradskyi or heterotrophic bacteria. Together, N. winogradskyi and heterotrophic bacteria reduced the oxidative stress for Nitrosomonas sp. Is79, which resulted in a more efficient metabolism.Importance Aerobic ammonia oxidizing microorganisms play an important role in the global nitrogen cycle, converting ammonia to nitrite. In their natural environment they coexist and interact with nitrite oxidizers, which convert nitrite to nitrate, and with heterotrophic microorganisms. The presence of nitrite oxidizers and heterotrophic bacteria has a positive influence on the growth of the ammonia oxidizers. Here we present a study investigating the effect of nitrite oxidizers and heterotrophic bacteria on the proteome of a selected ammonia oxidizer in a defined culture to elucidate how these two groups improve the performance of the ammonia oxidizer. The results show that the presence of nitrite oxidizers and heterotrophic bacteria reduced stress for the ammonia oxidizers and resulted in a more efficient energy generation. This study contributes to our understanding of microbe-microbe interactions, in particular between ammonia oxidizers and their neighboring microbial community.

KW - international

U2 - 10.1128/AEM.01171-16

DO - 10.1128/AEM.01171-16

M3 - Article

SN - 0099-2240

VL - 82

SP - 4776

EP - 4788

JO - Applied and Environmental Microbiology

JF - Applied and Environmental Microbiology

IS - 15

ER -

The effect of bacterial community members on the proteome of the ammonia-oxidizing bacterium Nitrosomonas sp. Is79

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