High-throughput proteomic profiling of the fish liver following bacterial infection

Dwight R Causey, Moritz A N Pohl, David A Stead, Samuel A M Martin, Christopher J Secombes, Daniel MacQueen (Corresponding Author)

Research output: Contribution to journalArticle

3 Citations (Scopus)
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Abstract

High-throughput proteomics was used to determine the role of the fish liver in defense responses to bacterial infection. This was done using a rainbow trout (Oncorhynchus mykiss) model following infection with Aeromonas salmonicida, the causative agent of furunculosis. The vertebrate liver has multifaceted functions in innate immunity, metabolism, and growth; we hypothesize this tissue serves a dual role in supporting host defense in parallel to metabolic adjustments that promote effective immune function. While past studies have reported mRNA responses to A. salmonicida in salmonids, the impact of bacterial infection on the liver proteome remains uncharacterized in fish.

Results
Rainbow trout were injected with A. salmonicida or PBS (control) and liver extracted 48 h later for analysis on a hybrid quadrupole-Orbitrap mass spectrometer. A label-free method was used for protein abundance profiling, which revealed a strong innate immune response along with evidence to support parallel rewiring of metabolic and growth systems. 3076 proteins were initially identified against all proteins (n = 71,293 RefSeq proteins) annotated in a single high-quality rainbow trout reference genome, of which 2433 were maintained for analysis post-quality filtering. Among the 2433 proteins, 109 showed significant differential abundance following A. salmonicida challenge, including many upregulated complement system and acute phase response proteins, in addition to molecules with putative functions that may support metabolic re-adjustments. We also identified novel expansions in the complement system due to gene and whole genome duplication events in salmonid evolutionary history, including eight C3 proteins showing differential changes in abundance.

Conclusions
This study provides the first high-throughput proteomic examination of the fish liver in response to bacterial challenge, revealing novel markers for the host defense response, and evidence of metabolic remodeling in conjunction with activation of innate immunity.
Original languageEnglish
Article number719
JournalBMC Genomics
Volume19
DOIs
Publication statusPublished - 1 Oct 2018

Fingerprint

Aeromonas salmonicida
Bacterial Infections
Proteomics
Fishes
Oncorhynchus mykiss
Liver
Innate Immunity
Proteins
Genome
Furunculosis
Salmonidae
Acute-Phase Reaction
Acute-Phase Proteins
Trout
Proteome
Growth
Vertebrates
History
Messenger RNA
Infection

Keywords

  • Label-free proteomics
  • Hybrid quadrupole-Orbitrap mass spectrometry
  • Immune System
  • Rainbow trout
  • Aeromonas salmonicida
  • Complement system
  • Complement C3
  • Gene duplication

Cite this

High-throughput proteomic profiling of the fish liver following bacterial infection. / Causey, Dwight R; Pohl, Moritz A N; Stead, David A; Martin, Samuel A M; Secombes, Christopher J; MacQueen, Daniel (Corresponding Author).

In: BMC Genomics, Vol. 19, 719, 01.10.2018.

Research output: Contribution to journalArticle

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abstract = "High-throughput proteomics was used to determine the role of the fish liver in defense responses to bacterial infection. This was done using a rainbow trout (Oncorhynchus mykiss) model following infection with Aeromonas salmonicida, the causative agent of furunculosis. The vertebrate liver has multifaceted functions in innate immunity, metabolism, and growth; we hypothesize this tissue serves a dual role in supporting host defense in parallel to metabolic adjustments that promote effective immune function. While past studies have reported mRNA responses to A. salmonicida in salmonids, the impact of bacterial infection on the liver proteome remains uncharacterized in fish.ResultsRainbow trout were injected with A. salmonicida or PBS (control) and liver extracted 48 h later for analysis on a hybrid quadrupole-Orbitrap mass spectrometer. A label-free method was used for protein abundance profiling, which revealed a strong innate immune response along with evidence to support parallel rewiring of metabolic and growth systems. 3076 proteins were initially identified against all proteins (n = 71,293 RefSeq proteins) annotated in a single high-quality rainbow trout reference genome, of which 2433 were maintained for analysis post-quality filtering. Among the 2433 proteins, 109 showed significant differential abundance following A. salmonicida challenge, including many upregulated complement system and acute phase response proteins, in addition to molecules with putative functions that may support metabolic re-adjustments. We also identified novel expansions in the complement system due to gene and whole genome duplication events in salmonid evolutionary history, including eight C3 proteins showing differential changes in abundance.ConclusionsThis study provides the first high-throughput proteomic examination of the fish liver in response to bacterial challenge, revealing novel markers for the host defense response, and evidence of metabolic remodeling in conjunction with activation of innate immunity.",
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author = "Causey, {Dwight R} and Pohl, {Moritz A N} and Stead, {David A} and Martin, {Samuel A M} and Secombes, {Christopher J} and Daniel MacQueen",
note = "Funding Proteomics research in DJM’s lab was supported by the Royal Society (grant ref.: RG130823) and the Biotechnology and Biological Sciences Research Council (grant ref.: BB/M026345/1). DRC’s PhD studentship is supported through The Developmental Trust and Elphinstone Scholarship Programme of the University of Aberdeen. Availability of data and materials All mass spectrometry proteomics data generated in the study was deposited to the ProteomeXchange Consortium via the PRIDE [135] partner repository with the dataset identifier PXD010186. All other data generated or analyzed during the study are included in this published article and its supplementary information files.",
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N1 - Funding Proteomics research in DJM’s lab was supported by the Royal Society (grant ref.: RG130823) and the Biotechnology and Biological Sciences Research Council (grant ref.: BB/M026345/1). DRC’s PhD studentship is supported through The Developmental Trust and Elphinstone Scholarship Programme of the University of Aberdeen. Availability of data and materials All mass spectrometry proteomics data generated in the study was deposited to the ProteomeXchange Consortium via the PRIDE [135] partner repository with the dataset identifier PXD010186. All other data generated or analyzed during the study are included in this published article and its supplementary information files.

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N2 - High-throughput proteomics was used to determine the role of the fish liver in defense responses to bacterial infection. This was done using a rainbow trout (Oncorhynchus mykiss) model following infection with Aeromonas salmonicida, the causative agent of furunculosis. The vertebrate liver has multifaceted functions in innate immunity, metabolism, and growth; we hypothesize this tissue serves a dual role in supporting host defense in parallel to metabolic adjustments that promote effective immune function. While past studies have reported mRNA responses to A. salmonicida in salmonids, the impact of bacterial infection on the liver proteome remains uncharacterized in fish.ResultsRainbow trout were injected with A. salmonicida or PBS (control) and liver extracted 48 h later for analysis on a hybrid quadrupole-Orbitrap mass spectrometer. A label-free method was used for protein abundance profiling, which revealed a strong innate immune response along with evidence to support parallel rewiring of metabolic and growth systems. 3076 proteins were initially identified against all proteins (n = 71,293 RefSeq proteins) annotated in a single high-quality rainbow trout reference genome, of which 2433 were maintained for analysis post-quality filtering. Among the 2433 proteins, 109 showed significant differential abundance following A. salmonicida challenge, including many upregulated complement system and acute phase response proteins, in addition to molecules with putative functions that may support metabolic re-adjustments. We also identified novel expansions in the complement system due to gene and whole genome duplication events in salmonid evolutionary history, including eight C3 proteins showing differential changes in abundance.ConclusionsThis study provides the first high-throughput proteomic examination of the fish liver in response to bacterial challenge, revealing novel markers for the host defense response, and evidence of metabolic remodeling in conjunction with activation of innate immunity.

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KW - Complement system

KW - Complement C3

KW - Gene duplication

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JO - BMC Genomics

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SN - 1471-2164

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