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High Nutrient Concentration Can Induce Virulence Factor Expression and Cause Higher Virulence in an Environmentally Transmitted Pathogen

Microbial Ecology volume 72, pages 955–964 (2016)Cite this article

Abstract

Environmentally transmitted opportunistic pathogens shuttle between two substantially different environments: outside-host and within-host habitats. These environments differ from each other especially with respect to nutrient availability. Consequently, the pathogens are required to regulate their behavior in response to environmental cues in order to survive, but how nutrients control the virulence in opportunistic pathogens is still poorly understood. In this study, we examined how nutrient level in the outside-host environment affects the gene expression of putative virulence factors of the opportunistic fish pathogen Flavobacterium columnare. The impact of environmental nutrient concentration on bacterial virulence was explored by cultivating the bacteria in various nutrient conditions, measuring the gene expression of putative virulence factors with RT-qPCR and, finally, experimentally challenging rainbow trout (Oncorhynchus mykiss) fry with these bacteria. Our results show that increased environmental nutrient concentration can increase the expression of putative virulence genes, chondroitinase (cslA) and collagenase, in the outside-host environment and may lead to more rapid fish mortality. These findings address that the environmental nutrients may act as significant triggers of virulence gene expression and therefore contribute to the interaction between an environmentally transmitted opportunistic pathogen and its host.

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Acknowledgments

The authors would like to thank Prof. Annemie Decostere for commenting on the manuscript and Ms Irene Helkala, Ville Hoikkala, MSc, Dr. Elina Laanto, Katja Neuvonen, MSc, Marjut Paljakka, MSc, Mr Petri Papponen, Dr. Katja Pulkkinen, and Dr. Ilona Rissanen, for assistance in the laboratory.

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Authors and Affiliations

  1. Department of Biological and Environmental Science and Nanoscience Center, University of Jyvaskyla, Center of Excellence in Biological Interactions, P.O. Box 35, FI-40014, University of Jyvaskyla, Jyvaskyla, Finland

    Reetta Penttinen, Hanna Kinnula, Jaana K. H. Bamford & Lotta-Riina Sundberg

  2. University of Eastern Finland, A.I. Virtanen Institute for Molecular Sciences, P.O. Box 1627, FI-70211, Kuopio, Finland

    Anssi Lipponen

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  1. Reetta Penttinen
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  2. Hanna Kinnula
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  3. Anssi Lipponen
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  4. Jaana K. H. Bamford
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  5. Lotta-Riina Sundberg
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Corresponding author

Correspondence to Reetta Penttinen.

Ethics declarations

The fish experiments were conducted according to the Finnish Act on Use of Animals for Experimental Purposes, under permission ESAVI-3940/04.10.07/2015 granted for L-RS by the National Animal Experiment Board at the Regional State Administrative Agency for Southern Finland.

Funding Information

This work was funded by Academy of Finland grant nos. 252411 (the Centre of Excellence in Biological Interactions 2012–2017) and 272995 (for L-RS), Maj and Tor Nessling Foundation, and the Doctoral Programme in Biological and Environmental Science (University of Jyväskylä). The funders had no role in study design, data collection, and interpretation, or the decision to submit the work for publication in Microbial Ecology.

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The authors declare that they have no conflict of interest.

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Penttinen, R., Kinnula, H., Lipponen, A. et al. High Nutrient Concentration Can Induce Virulence Factor Expression and Cause Higher Virulence in an Environmentally Transmitted Pathogen. Microb Ecol 72, 955–964 (2016). https://doi.org/10.1007/s00248-016-0781-1

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  • DOI: https://doi.org/10.1007/s00248-016-0781-1

Keywords

  • Chondroitinase
  • Collagenase
  • Colony type
  • Flavobacterium columnare
  • Nutrients
  • RT-qPCR
  • Virulence factors