My research interest lies in the interactions between bacteria and their plant hosts. The research is primarily focused on food-borne bacteria, but also covers opportunistic plant pathogens because of the many similarities in the types of interactions; transmission of the bacteria through the wider environment and the plant host response.
Biography
Pathogenic enterobacteria Escherichia coli, Salmonella enterica and Klebsiella pneumoniae are normally associated with animal reservoirs. However, a significant proportion of food poisoning outbreaks are attributable to fresh produce (fresh fruit and vegetables). We have good evidence to show that the bacteria are not transported by the plant in an inert manner, rather they interact with plant hosts at a molecular level and are able to replicate both on external and internal plant tissue. Comparative genomics has shown that enteric human pathogens are closely related to enteric plants pathogens, in particular Pectobacterium spp. (formerly Erwinia) (sequenced by Ian Toth and colleagues: Bell et al., 2004 PNAS 101:11105). The comparison allows identification of key genes that are involved in interactions with plants, at the first step of adherence and the subsequent steps of invasion and persistence.
The research on food-borne pathogens investigates bacterial factors required for different stages of colonisation, as well as the plant response. We also investigate transmission of bacteria in agricultural systems, from soil amendments to harvested crops. Projects with plant pathogenic bacteria are on-going to find alternative treatment options to current bactericides. The over-all aim of the research is to gain a better understanding of the mechanisms that govern bacteria-plant interactions, with the goal of reducing human illness and plant disease.
Research
Externally funded research projects
- Identification and characterisation of EHEC adherence factors that interact with plant tissue. Funded by the BBSRC, Oct 2011 – Sept 2014
- Transcriptome analysis of enterohaemorrhagic Escherichia coli in planta. Jointly funded by the James Hutton Institute and the University of Reading, Oct 2011 – Sept 2014
- Defining the interactions between plant cell walls and bacterial surface factors. Funded by the Leverhulme Trust, Feb 2012 – Jan 2015
Other projects funded by RESAS investigate aspects of the plant host response to zoonotic bacteria as well as the population genetics of plant and environmental isolates of Escherichia coli.
Past research
Previous research has focused on the regulation of bacterial factors that enable them to adapt to different hosts and environments.
Collaborators
- At the James Hutton Institute with partners in Environmental and Biochemical Sciences and in Controlling Weeds, Pests and Diseases research theme.
- Professor David L. Gally; Dr Maurice P. Gallagher (University of Edinburgh)
- Dr Thamarai Schneiders (University of Belfast)
- Professor Dale Walters (SAC)
- Dr Rob Jackson (University of Reading)
- Dr Ruth Zadocks (Moredun Research Institute)
Publications
Journals
- Wright, K.M.; Marshall, J.; Wright, P.J.; Holden, N.J. (2023) Vacuolar localisation of anthocyanin pigmentation in microgreen cotyledons of basil, cabbage and mustard greens does not impact on colonisation by Shiga-toxigenic Escherichia coli O157:H7, Food Microbiology, 116, Art. 104367
- Engelhardt, I.; Patko, D.; Liu, Y.; Mimault, M.; de las Heras Martinez, G.; George, T.; Macdonald, M.; Ptashnyk , M.; Sukhodub, T.; Stanley-Wall, N.; Holden, N.; Daniell, T.; Dupuy , L. (2022) Novel form of collective movement by soil bacteria, The ISME Journal, 16, 2337-2347
- Crozier, L.; Marshall, J.; Holmes, A.; Wright, K.; Rossez, Y.; Merget, B.; Humphris, S.; Toth, I.; Jackson, R.W.; Holden, N. (2021) The role of l-arabinose metabolism for Escherichia coli O157:H7 in edible plants, Microbiology Society, 167(7)
- Yassin, M.; Ton, J.; Rolfe, S.A.; Valentine, T.A.; Cromey, M.; Holden, N.J.; Newton, A.C. (2021) The rise, fall and resurrection of chemical-induced resistance agents., Pest Management Science, 77, 3900-3909
- Wright, K.; Wright, P.; Holden, N.J. (2021) MacConkey broth purple provides an efficient MPN estimation method for Shigatoxigenic Escherichia coli. , Journal of Microbiological Methods, 181, Article No. 106132
- De Vega, D.; Holden, N.; Hedley, P.E.; Morris, J.; Luna, E.; Newton, A.C. (2021) Chitosan primes plant defence mechanisms against Botrytis cinerea, including expression of Avr9/Cf-9 rapidly-elicited genes., Plant, Cell and Environment, 44(1), 290-303
- Holmes, A.; Rossez, Y.; Wright, K.M.; Hedley, P.E.; Morris, J.; Willats, W.G.T.; Holden, N.J. (2020) Esherichia coli O157:H7 F9 fimbriae recognize plant xyloglucan and elicit a response in Arabidopsis thaliana., International Journal of Molecular Sciences, 21, Article No. 9720.
- Holmes, A.; Pritchard, L.; Hedley, P.; Morris, J.; McAteer, S.P.; Gally, D.L.; Holden, N.J. (2020) A high-throughput genomic screen identifies a role for the plasmid-borne type II secretion system of Escherichia coli O157:H7 (Sakai) in plant-microbe interactions., Genomics, 112, 4242-4253.
- Carroll, D.; Holden, N.J.; Gifford, M.L.; Dupuy, L.X. (2020) Framework for quantification of the dynamics of root colonization by Pseudomonas fluorescens isolate SBW25, Frontiers in Microbiology, 11, Article No. 585443
- Holmes, A.; Pritchard, L.; Hedley, P.; Morris, J.; McAteer, S.P.; Gally, D.L.; Holden, N.J. (2020) Dataset of Escherichia coli O157:H7 genes enriched in adherence to spinach root tissue., Data in Brief, 31, Article No. 105769.
- Schikora, A.; Jackson, R.W.; Van Overbeek, L.; Holden, N.J. (2020) Editorial: Plants as alternative hosts for human and animal pathogens – second edition., Frontiers in Microbiology, 11, Article No. 1439.
- Holden, N.J.; Kredics, L.; Barak, J. (2020) Thematic issue on human pathogens in the environment: biology and risk factors., FEMS Microbiology Letters, 367, Article No. fnaa068.
- Merget, B.; Dobrinde, U.; Forbes, K.J.; Strachan, N.J.C.; Brennan, F.; Holden, N.J. (2020) Variability in growth responses of non-O157 EHEC isolates in leafy vegetables, sprouted seeds and soil extracts occurs at the isolate level., FEMS Microbiology Letters, 367, Article No. fnaa030.
- Holden, N.J. (2019) You are what you can find to eat: bacterial metabolism in the rhizosphere., Current Issues in Molecular Biology, 30, 1-16.
- Merget, B.; Forbes, K.J.; Brennan, F.; McAteer, S.; Shepherd, T.; Strachan, N.J.; Holden, N.J. (2019) Influence of plant species, tissue type, and temperature on the capacity of shiga-toxigenic escherichia coli to colonize, grow, and be internalized by plants., Applied and Environmental Microbiology, 85, Article No. UNSP e00123-19.
- Grabowiecka, E.; Martin, D.; Crozier, L.; Holden, N.J. (2019) Escherichia coli O157:H7 transcriptome datasets for comparison of RNA-seq and microarray platforms., Data in Brief, 22, 126-131.
- Wright, K.; Holden, N.J. (2018) Quantification and colonisation dynamics of Escherichia coli O157:H7 inoculation of microgreens species and plant growth substrates., International Journal of Food Microbiology, 273, 1-10
- Lupolova, N.; Dallman, T.J.; Holden, N.J.; Gally, D.L. (2017) Patchy promiscuity: machine learning applied to predict the host specificity of Salmonella enterica and Escherichia coli., Microbial Genomics, 3, Article No. 000135.
- Wright, K.M.; Crozier, L.; Marshall, J.; Merget, B.; Holmes, A.; Holden, N.J. (2017) Differences in internalisation and growth of Escherichia coli O157:H7 within the apoplast of edible plants, spinach and lettuce, compared with the model species Nicotiana benthamiana., Microbial Biotechnology, 10, 555-569.
- Marshall, J.; Rossez, Y.; Mainda, G.; Gally, D.L.; Daniell, T.J.; Holden, N.J. (2016) Alternate thermoregulation and functional binding of Escherichia coli type 1 fimbriae in environmental and animal isolates., FEMS Microbiology Letters, 363, Article No. fnw251.
- Crozier, L.; Hedley, P.E.; Morris, J.; Wagstaff, C.; Andrews, S.C.; Toth, I.; Jackson, R.W.; Holden, N. (2016) Corrigendum: whole-transcriptome analysis of verocytotoxigenic Escherichia coli O157:H7 (Sakai) suggests plant-species-specific metabolic responses on exposure to spinach and lettuce extracts., Frontiers in Microbiology, 7, Article No. 1506.
- Crozier, L.; Hedley, P.E.; Morris, J.; Wagstaff, C.; Andrews, S.C.; Toth, I.; Jackson, R.W.; Holden, N. (2016) Whole-transcriptome analysis of verocytotoxigenic Escherichia coli O157:H7 (Sakai) suggests plant-species-specific metabolic responses on exposure to spinach and lettuce extracts., Frontiers in Microbiology, 7, Article No. 1088.
- Van der Linden, I.; Cottyn, B.; Uyttendaele, M.; Vlaemynck, G.; Heyndrickx, M.; Maes, M.; Holden, N. (2016) Microarray-based screening of differentially expressed genes of e. coli O157:H7 sakai during preharvest survival on butterhead lettuce., Agriculture-Basel, 6, Article No. 6.
- Holden, N.J.; Jackson, R.W.; Schikora, A. (2015) Editorial on plants as alternative hosts for human and animal pathogens., Frontiers in Microbiology, 6, Article No. 397.
- Rossez, Y.; Wolfson, E.B.; Holmes, A.; Gally, D.L.; Holden, N.J. (2015) Bacterial flagella: twist and stick, or dodge across the Kingdoms., PLoS Pathogens, 11, Article No. e1004483.
- Rossez, Y.; Holmes, A.; Lodberg-Pedersen, H.; Birse, L.; Marshall, J.; Willats, W.G.T.; Toth, I.K.; Holden, N.J. (2014) Escherichia coli common pilus (ECP) targets arabinosyl residues in plant cell walls to mediate adhesion to fresh produce plants., Journal of Biological Chemistry, 289, 34349-34365.
- Holmes, A.; Birse, L.; Jackson, R.W.; Holden, N.J. (2014) An optimised method for the extraction of bacterial mRNA from plant roots infected with Escherichia coli O157:H7., Frontiers in Microbiology, 5, Article No. 286.
- Rossez, Y.; Holmes, A.; Wolfson, W.B.; Gally, D.L.; Mahjan, A.; Pedersen, H.L.; Willats, W.G.T.; Toth, I.K.; Holden, N. (2014) Flagella interact with ionic plant lipids to mediate adherence of pathogenic Escherichia coli to fresh produce plants., Environmental Microbiology, 16, 2181-2195.
- Holden, N.J.; Wright, F.; MacKenzie, K.; Marshall, J.; Mitchell, S.; Mahajan, A.; Wheatley, R.; Daniell, T.J. (2014) Prevalence and diversity of Escherichia coli isolated from a barley trial supplemented with bulky organic soil amendments: green compost and bovine slurry., Letters in Applied Microbiology, 58, 205-212.
- Wright, K.M.; Chapman, S.N.; McGeachy, K.; Humphris, S.; Campbell, E.; Toth, I.K.; Holden, N.J. (2013) The endophytic lifestyle of Escherichia coli O157:H7: quantification and internal localization in roots., Phytopathology, 103, 333-340.
Books / chapters
- Holden, N.J. (2021) How Can Plant Pathology Help in the Control of Human Pathogens Associated with Edible Crop Plants?, In: Scott, P., Strange, R., Korsten, L. & Gullino, M.L. (eds.). Plant Diseases and Food Security in the 21st Century. Plant Pathology in the 21st Century, Volume 10. Cham: Springer, Chapter 13, pp 259-275
- Rossi, C.; Cazzola, H.; Holden, N.J.; Rossez, Y. (2019) Bacterial Adherence to Plant and Animal Surfaces Via Adhesin-Lipid Interactions, In: Goldfine H. (ed.) Health Consequences of Microbial Interactions with Hydrocarbons, Oils, and Lipids. Handbook of Hydrocarbon and Lipid Microbiology . Springer: Cham, 1-21
- Holden, N.J. (2018) You are what you can find to eat: bacterial metabolism in the rhizosphere, In: Schikora, A. (ed.) Plant-Microbe Interactions in the Rhizosphere. Caister Academic Press, 1-16
- Holden, N.J.; Holmes, A.; Rossez, Y. (2015) The molecular interactions between human pathogenic bacteria and plants., In: Murillo, J., Vinatzer, B.A., Jackson, R.W. & Arnold, D.L. (eds.). Bacteria-Plant Interactions: Advanced Research and Future Trends, Caister Academic Press, pp139-166.
- Holden, N.; Pritchard, L.; Toth, I.K.; Wright, K.M. (2013) Mechanism of plant colonisation by human pathogenic enterobacteria: an emphasis on the roots and rhizosphere., In: de Bruijn, F. (ed.). Molecular Microbial Ecology of the Rhizosphere. Wiley Blackwell, Hoboken, New Jersey, Volume 2, Chapter 117, pp1217-1226.
Technical / contract reports
- Holden, N.; Newton, A.C.; Walters, D. (2015) Use of plant defence elicitors to provide induced resistance protection in brassica and allium crops., Annual Report on HDC Project FV417.
- Holden, N.; Toth, I.K.; Newton, A.C.; Walters, D. (2012) Assessment of plant elicitors to induce resistance against head-rot in broccoli., HDC Annual Report 2012.
- Holden, N.; Toth, I.K.; Newton, A.C. (2012) Reducing bacterial infection in seed onions through the use of plant elicitors., HDC Grower Summary, FV393, Final 2012.
- Holden, N. (2010) Enterobacteria survival on plants: implications for food safety., Annual Report of the Scottish Crop Research Institute for 2009, pp34-35.
Conference papers
- Holmes, A.; Stanley-Wall, N.; Newton, A.; Holden, N.J. (2018) Can plant growth-promoting rhizobacteria be used to control bacterial pathogens on horticultural produce?, Crop Protection in Northern Britain 2018: The Dundee Conference, Environmental Management and Crop Production, Apex City Quay Hotel, Dundee, 27-28 February 2018. Conference Proceedings, 59-64.
- Newton, A.C.; Reglinski, T.; De Vega Perez, D.; Holden, N.H.; Wiesel, L.; Gravouil, C.; Bain, R.; Havis, N.; Walters, D.R. (2016) Elicitors: what is available and can we optimise their potential benefits?, BCPC Diseases Review, NIAB, Cambridge, 7 December 2016.
- Adu, M.; Marshall, J.; Newton, A.C.; Holden, N. (2016) Harpin confers some protection against bacterial pathogens of horticultural crops., The Dundee Conference: Crop Protection in Northern Britain 2016, Dundee, 23-24 February 2016, pp35-42.
- Holden, N. (2014) New research on E. coli O157 shows how pathogenic E. coli O157:H7 binds to fresh vegetables., Society for General Microbiology (SGM) Annual Conference, Arena and Convention Centre, Liverpool, 14-17 April 2014.
- Newton, A.C.; Holden, N.; De Vega Perez, D.; Gravouil, C.; Walters, D.R. (2014) Induced resistance in crop protection: an overview., Integrated Control in Protected Crops, Temperate Climate, IOBC-WPRS Bulletin, 102, 169-174.
- Holden, N.; Okpo, A.; Newton, A.C.; Walters, D.R. (2014) Application of plant defence elicitors on horticultural crops to control bacterial pathogens., Crop Protection in Northern Britain, Environmental Management and Crop Protection, West Park Conference Centre, Dundee, 25-26 February 2014.
- Holden, N.J.; Toth, I.K.; Newton, A.C. (2013) Can plant defence elicitors control bacterial infection in field vegetables?, In: Bardin, M., Mauch-Mani, B., Mazzotta, S., Nicot, P., Pieterse, C., Poessel, J-L., Ponchet, M. & Schmitt, A. (eds.). Induced Resistance in Plants against Insects and Diseases – Leaping from Success in the Lab to Success in the Field. Proceedings of the IOBC/WPRS, Avignon, France, 10-13 June 2013. IOBC-WRS Bulletin, 89, 433-443.
- Holden, N.J.; Toth, I.K.; Newton, A.C.; Walters, D. (2012) The use of plant elicitors in the control of bacterial infection in field vegetables., Proceedings Crop Protection in Northern Britain, Dundee, 28-29 February, 2012, pp175-180.
- Toth, I.K.; Holden, N.; Pritchard, L. (2012) Genomics research on Pectobacterium and Dickeya species: disease, ecology and diagnosis., Molecular Plant Microbe Interactions (MPMI) Conference, Kyoto, Japan, 27 July 2012.
- Toth, I.K.; Holden, N.; Pritchard, L. (2012) We only find what we look for: can enteric pathogens of animals live on and be spread by plants?, KNVM/NVMM Dutch Microbiology Society, Papendal, the Netherlands, 17 April 2012.
- Newton, A.C.; Toth, I.K.; Holden, N. (2011) Implications of climate change for pathogen defence in plants., Society for General Microbiology Spring Conference, Harrogate, 11-14 April 2011. HA09 Food Bio Security Session. (Abstract).
Conference posters / abstracts
- Holmes, A.; Wright, K.; Marshall, J.; Holden, N. (2019) The lush life: Escherichia coli O157 colonising the apoplast., MPMI 2019, XVIII Congress, Glasgow, 14-18 July 2019. Molecular Plant-Microbe Interactions, 32, 109. (Poster).
- Holden, N.J.; Marshall, J.; Valentine, T.A.; Newton, A. (2018) Relating tillage management systems of barley to rhizosphere composition and fungal disease., International Phytobiomes Conference 2018, Montpellier, France, 4-6 December 2018. (Poster)
- Holmes, A.; Rossez, Y.; Hedley, P.; Morris, J.; Gally, D.; Holden, N.J. (2018) I’ll stick to the salad: mechanisms of VTEC adherence to fresh leafy produce., Microbiology Society Annual General Meeting, International Conference Centre (ICC), Birmingham, 10-13 April 2018. Poster Abstract Book, P490.
- Holmes, A.; Marshall, J.; Wright, K.; Holden, N.J. (2018) I’ll stick to the salad: Adherence mechanisms of VTEC to salad crops., 10th International Symposium on Shiga Toxin (Verocytotoxin) Producing Escherichia coli Infections, Florence, Italy, 6-9 May 2018.
- Wright, K.; Marshall, J.; Holmes, A.; Holden, N.J. (2018) Entertaining with E coli O157., Frontiers in BioImaging Meeting, Glasgow, 27-28 June 2018. Abstract.
- Holmes, A.; Newton, A.; Stanley-Wall, N.R.; Holden, N.J. (2018) Can plant growth-promoting rhizobacteria be used to control bacterial pathogens on horticultural produce?, Crop Protection in Northern Britain 2018: The Dundee Conference, Environmental Management and Crop Production, Apex City Quay Hotel, Dundee, 27-28 February 2018. Conference Proceedings, pp59-64.
- Holmes, A.; Kalamara, M.; Stanley-Wall, N.R.; Holden, N.J. (2017) Can fresh produce be protected from colonisation by human pathogens through the application of plant growth promoting rhizobacteria (PGPR) as biocontrol?, 7th Congress of European Microbiologists (FEMS 2017), Valencia, Spain, 9-13 July 2017, Abstract No 189.
- Holmes, A.; Kalamara, M.; Stanley-Wall, N.R.; Holden, N.J. (2017) Can plant growth promoting rhizobacteria (PGPR) be applied as biocontrol to protect fresh produce from colonisation by human pathogens?, Microbiology Society Annual General Meeting, Edinburgh, 10-13 April 2017. Abstract No.475.
- Holmes, A.; Hedley, P.; Morris, J.; Rossez, Y.; Toth, I.; Holden, N.J. (2017) There’s something hairy going on: Understanding the defence response of plants to Escherichia coli O157:H7., Microbiology Society Annual General Meeting, Edinburgh, 3-6 April 2017.
- Wright, K.M.; Crozier, L.; Marshall, J.; Merget, B.; Holmes, A.; Holden, N.J. (2017) Differences in internalisation and growth of Escherichia coli O157_H7 within the apoplast of edible plants, spinach and lettuce, compared with the model species Nicotiana benthamiana., Microbiology Society Annual Meeting, Edinburgh, 3-6 April 2017. (Poster)
- Holmes, A.; Hedley, P.; Morris, J.; Holden, N.J. (2016) Understanding the defence response of plants to Escherichia coli O157:H7., Young Microbiologists Symposium on Microbe Signalling, Organisation and Pathogenesis, Apex Hotel, Dundee, 29-30 June 2016. Poster session I. No. 5.
- Wright, K.M.; Marshall, J.; Holmes, A.; Holden, N.J. (2016) E coli O157:H7 – Watch out for the salad as well as the undercooked beefburger!, Young Microbiologists Symposium on Microbe Signalling, Organisation and Pathogenesis 2016, Apex City Quay Hotel, Dundee, 29-30 June 2016.
- Brennan, F.P.; Pritchard, L.; Holden, N.M.; Abram, F. (2014) Exploring the genomic and phenotypic basis for E.coli naturalisation in soil., In: Cooperative of Zoonoses Experience and Expertise (CoZEE) Conference: The Role of High-throughput Sequencing in Surveillance, Diagnostics and Tracking Zoonotic Bacteria, The James Hutton Institute, Dundee, 11-12 November 2014.
- Holden, N.; Birse, L.; Marshall, J.; Rossez, Y.; Holmes, A. (2013) Molecular interactions between food-borne bacteria and plant hosts., EMBO/EMBL Symposia, New Approaches and Concepts in Microbiology, Heidelberg, Germany, 14-16 October 2013.
- Holden, N.J.; Daniell, T.; Marshall, J. (2013) Root and soil-borne Escherichia coli isolates express type 1 fimbriae at low temperature., BSSS Rhizosphere Interactions, A one day Symposium, the James Hutton Institute, Dundee, 18 March 2013.
- Holden, N.J.; Newton, A.C.; Toth, I.K.; Walters, D. (2012) Induced plant defence to fight pathogens., British Science Festival Exhibition, Aberdeen, 21 September 2012.
- Holden, N.; Toth, I.K.; Newton, A.C.; Walters, D. (2012) The use of plant elicitors in the control of bacterial infection in field vegetables., The Dundee Conference. Crop Protection in Northern Britain, Dundee, 28-29 February 2012 pp175-180.
- Rossez, Y.; Holmes, A.; Ahl, L.I.; Pedersen, H.L.; Willats, W.G.T.; Toth, I.; Holden, N. (2012) Role of bacterial surface factors in adherence of enteric bacteria to plant polysaccharide., Glycobiology, 22, 1638.
- Holden, N.; Toth, I.K.; Newton, A.C.; Walters, D. (2012) The use of plant elicitors in the control of bacterial infection in field vegetables., Crop Protection of Northern Britain, Environmental Management and Crop Protection, The Dundee Conference, The West Park Conference Centre, Dundee, 28-29 February 2012. (Poster)
- Holden, N.; Toth, I.K.; Walters, D.; Newton, A.C. (2011) Plant defence elicitors as a means to control opportunistic plant pathogenic bacteria., Annual BSPP Meeting, Cambridge, 15-17 December 2011. (Poster)