Nicola Holden
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.
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.
Current research interests
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)
Bibliography
- Yassin, M.; Ton, J.; Rolfe, S.A.; Valentine, T.A.; Cromey, M.; Holden, N.J.; Newton, A.C. (In press) The rise, fall and resurrection of chemical-induced resistance agents., Pest Management Science.
- Rossi, C.; Cazzola, H.; Holden, N.J.; Rossez, Y. (In press) Bacterial adherence to plant and animal surfaces via adhesin-lipid interactions., In: Goldfine H. (eds). Health Consequences of Microbial Interactions with Hydrocarbons, Oils, and Lipids. Handbook of Hydrocarbon and Lipid Microbiology. Springer, Cham, Switzerland, Chapter,
- 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, 290-303.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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
- 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, Chapter 1, pp1-16.
- 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.
- 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.
- 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.
- 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.
- 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.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.
- 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.; 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.
- 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.
- 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.
- Newton, A.C.; Torrance, L.; Holden, N.; Toth, I.K.; Cooke, D.E.L.; Blok, V.C.; Gilroy, E.M. (2012) Chapter three - climate change and defence against pathogens in plants., Advances in Applied Microbiology, 81, 89-132.
- Pritchard, L.; Holden, N.J.; Bielaszewska, M.; Karch, H.; Toth, I.K. (2012) Alignment-free design of highly discriminatory diagnostic primer sets for Escherichia coli O104:H4 outbreak strains., PLoS ONE, 7, Article No. e34498.
- Downie, H.; Holden, N.; Otten, W.; Spiers, A.J.; Valentine, T.A.; Dupuy, L.X. (2012) Transparent soil for imaging the rhizosphere., PLoS ONE, 7, Article No. e44276.
- 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) Plants as reservoirs for human enteric pathogens., CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources, 5(047), pp1-11.
- Holden, N. (2010) Enterobacteria survival on plants: implications for food safety., Annual Report of the Scottish Crop Research Institute for 2009, pp34-35.
- Holden, N.; Pritchard, L.; Toth, I.K. (2008) Colonisation outwith the colon: plants as an alternative environmental reservoir for human pathogenic enterobacteria., FEMS Microbiology Reviews, 33, 689-703.
- 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, 290-303.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.
- 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.; 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.
- 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.
- Newton, A.C.; Torrance, L.; Holden, N.; Toth, I.K.; Cooke, D.E.L.; Blok, V.C.; Gilroy, E.M. (2012) Chapter three - climate change and defence against pathogens in plants., Advances in Applied Microbiology, 81, 89-132.
- Pritchard, L.; Holden, N.J.; Bielaszewska, M.; Karch, H.; Toth, I.K. (2012) Alignment-free design of highly discriminatory diagnostic primer sets for Escherichia coli O104:H4 outbreak strains., PLoS ONE, 7, Article No. e34498.
- Downie, H.; Holden, N.; Otten, W.; Spiers, A.J.; Valentine, T.A.; Dupuy, L.X. (2012) Transparent soil for imaging the rhizosphere., PLoS ONE, 7, Article No. e44276.
- Holden, N. (2010) Plants as reservoirs for human enteric pathogens., CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources, 5(047), pp1-11.
- Holden, N.; Pritchard, L.; Toth, I.K. (2008) Colonisation outwith the colon: plants as an alternative environmental reservoir for human pathogenic enterobacteria., FEMS Microbiology Reviews, 33, 689-703.
- Holden, N.J.; Smith, D.G.E. (2014) CoZEE Conference 2014, (Conference organisation & co-chair)., CoZEE Zoonoses Network Autumn Conference: The Role of High-throughput Sequencing in Surveillance, Diagnostics and Tracking Zoonotic Bacteria, the James Hutton Institute, 11-12 November 2014.
- 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, Chapter 1, pp1-16.
- 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.
- 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.