Applied Soil Ecology 167 (2021) 104040 Contents lists available at ScienceDirect Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil Phytoremediation of microbial contamination in soil by New Zealand native plants Maria Jesus Gutierrez-Gines a,*, Hossein Alizadeh b, Elizabeth Alderton a, Vikki Ambrose a,1, Alexandra Meister c, Brett H. Robinson c, Sky Halford a,2, Jennifer A. Prosser a,3, Jacqui Horswell a,4 a Institute of Environmental Science and Research (ESR) Ltd., 34 Kenepuru Drive, Kenepuru, Porirua 5022, New Zealand b Bio-Protection Research Centre, PO Box 85084, Lincoln University, 7647 Canterbury, New Zealand c School of Physical and Chemical Sciences, University of Canterbury, 20 Kirkwood Ave, Christchurch 8041, New Zealand ARTICLE INFO ABSTRACT Keywords: Novel research has demonstrated that the roots of some bioactive plants - called pathogen phytoremediation Myrtaceae plants - enhance die-off of pathogenic organisms in the soil. Strategic establishment of pathogen phytor­ Winteraceae emediation plants may reduce the transport of human pathogens to water sources. Such plantings could be used Escherichia coli in riparian margins, as buffer strips to protect drinking water supplies, or block planting in ‘critical source areas’ Staphylococcus aureus of microbial contamination, such as grazing paddocks, organic waste – including sewage sludge - amended land, Pseudomonas aeruginosa Burkholderia cepacia animal feedlots and housing facilities, and manure storage areas. This work aimed to investigate the antimi­ crobial activity of a range of New Zealand native plants known for their antimicrobial potential from previous research or through indigenous knowledge, and to assess if any of them could potentially be used for pathogen phytoremediation. Two laboratory screening experiments demonstrated the antimicrobial activity of Lep­ tospermum scoparium, including the local variety swamp manuka,¯ Kunzea ericoides, Pseudowintera colorata, and Metrosideros robusta against three human pathogens and two indicator organisms. A greenhouse experiment showed a 90% reduction of Escherichia coli numbers in dairy shed effluent irrigated pots after 14 days in soils under swamp L. scoparium and M. robusta, compared with 45 days in soil under Lolium perenne. The pH in the soil under swamp L. scoparium and M. robusta was significantly lower than under L. perenne, which could partially explain the faster E. coli reduction. 1. Introduction development of pathogens with antibiotic resistance is pushing re­ searchers to find new antibiotic products and compounds (Gorlenko Medicinal use of plants is as old as humanity, with the first written et al., 2020). records of plant medicinal use dating from 2600 BC in Mesopotamia Recent novel research has investigated the use of medicinal plants to (Gurib-Fakim, 2006). Medicinal plants were also the first source of inhibit or kill human pathogens in the soil. Yossa et al. (2010) demon­ pharmaceuticals; Aspirin, produced from salicin extracted from bark of strated the efficacyof treating soil with essential oils from different plant Salix alba, was one of the firstexamples of a plant derived drug (McRae species to reduce contamination of food by Escherichia coli (E. coli) O157: et al., 2007). Bioprospecting, the process of discovery and commerci­ H7 in organic agriculture. Prosser et al. (2016) demonstrated a faster alisation of new products from biological resources, has become an die-off of E. coli under soil containing bioactive plants compared with important discipline, above all in the search for new drugs to treat soil planted with pasture only, and suggested the release of antimicro­ human diseases and/or conditions (McRae et al., 2007). Currently, the bial compounds as a probable mechanism. These authors were the first * Corresponding author. E-mail address: [email protected] (M.J. Gutierrez-Gines). 1 Present address: Nelson City Council, 110 Trafalgar Street, Nelson 7010, New Zealand. 2 Present address: School of Physical and Chemical Sciences, University of Canterbury, 20 Kirkwood Ave, Christchurch 8041, New Zealand. 3 Present address: Lowe Environmental Impact, 441 Church Street, Palmerston North 4410, New Zealand 4 Present address: Ministry for Primary Industries, PO Box 2526, Wellington 6140, New Zealand. https://doi.org/10.1016/j.apsoil.2021.104040 Received 24 November 2020; Received in revised form 6 April 2021; Accepted 14 April 2021 Available online 21 April 2021 0929-1393/© 2021 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). M.J. Gutierrez-Gines et al. Applied Soil Ecology 167 (2021) 104040 ones to refer to this research as phytoremediation of microbial 2. Materials and methods contamination. Contamination of soil by pathogenic microorganisms can occur via 2.1. Screening plants for antimicrobial potential many pathways including: excrements deposited by grazing livestock, land application of organic waste – including manure or sewage effluent, 2.1.1. Plant selection and plant extract preparation the use of animal products as soil conditioners, animal feedlots and The criteria considered to select the plants (Table 1) for this study housing facilities, and manure storage areas (Unc and Goss, 2004; Nicholson et al., 2005; Mosaddeghi et al., 2009; Semenov et al., 2009; Horswell et al., 2010; Ongeng et al., 2015). Horswell et al. (2010) Table 1 demonstrated that the presence of organic matter increases the survival List of plants tested for potential antimicrobial activity. Names and families of period of pathogens in the soil. This suggests that pathways of microbial plant species were checked October 2020 in www.nzflora.info. contamination that include high concentration of organic matter - such Scientific name Vernacular Family Reasons for selection as manures, organic waste, or dairy effluent- might be high risk settings name for sources of pathogens to other systems, like waterways. Phormium tenax J. Harakeke, Asphodelaceae Multiple medicinal uses, The transport of microbial contaminants to water sources signifi­ R.Forst. & G. flax many of them against cantly impacts water quality and is a major public health concern Forst infections and used as rongoa¯ by Maori¯ (Jones, worldwide (WHO, 2015). Ingestion of contaminated water, or food 2007; MWLR, 2020). irrigated with contaminated water can cause a variety of infectious Olearia paniculata Akiraho, Compositae Some Olearia species are water-borne diseases (Cooley et al., 2007; Pachepsky et al., 2011). (J.R.Forst. & G. golden poisonous (Crowe, Diarrhoeal disease caused by food and water contamination causes over Forst.) Druce akeake 2004). Kunzea ericoides Kanuka,¯ tea Myrtaceae Multiple medicinal uses, 1.8 million deaths per year (WHO, 2015). In 2016 in New Zealand, the (A.Rich.) Joy tree many of them against contamination of a drinking-water supply with Campylobacter jejuni by Thomps. infections (MWLR, run-off from an adjacent sheep farm infected over 8000 people (Gilpin 2020). et al., 2020). Strategic establishment of plants with antimicrobial Leptospermum Manuka,¯ tea Myrtaceae Multiple medicinal uses, properties in the root systems (pathogen phytoremediation plants) may scoparium J.R. tree many of them against Forst. & G. infections and used as reduce the transport of human pathogens from contaminated soils to Forst. rongoa¯ by Maori¯ (Jones, water sources through their use in riparian margins, block planting in 2007; MWLR, 2020). ‘critical source areas’ of microbial contamination, or even as buffer Leptospermum Swamp Myrtaceae Local variety of ¯ strips to protect drinking water supplies. scoparium J.R. manuka L. scoparium that grows Forst. & G. in swamp areas in the The Myrtaceae plant species from New Zealand (Leptospermum sco­ Forst. Lower Waikato region parium and Kunzea spp.) has demonstrated enhanced E. coli die-off in soil and it is recognized by (Prosser et al., 2016) and are well known for their antimicrobial prop­ local indigenous tribes erties through use in wound care products and as topical agents. These to have healing species have a high economic value, producing honey, oil, and cosmetics properties, probably even stronger than other which are sold widely throughout the world (Perry et al., 1997; Weston varieties (personal et al., 2000; Stephens et al., 2005; Adams et al., 2008). Potential eco­ communication from nomic return provides an extra incentive for their planting. Different Nga¯ Muka Development plant species have antimicrobial activity against different types of Trust and Matahuru Marae). pathogenic organisms (Calder et al., 1986). If plantations for pathogen Metrosideros Rat¯ a,¯ Myrtaceae Multiple medicinal uses, phytoremediation were to be used, a high biodiversity in such planta­ robusta A.Cunn northern many of them against tions would likely increase the spectrum of targeted organisms. In rata infections and used as addition, higher biodiversity would better represent native ecosystems rongoa¯ by Maori¯ (Jones, and diversify the root system structure, thus increasing the infiltrationof 2007; MWLR, 2020). Piper excelsum G. Kawakawa Piperaceae Multiple medicinal uses, run-off (Bharati et al., 2002) or even provide a wider range of ecosystem Forst. many of them against services (Gilvear et al., 2013). infections and used as Due to the high rate of endemism in New Zealand, 80% of the plant rongoa¯ by Maori¯ (Jones, species are not found anywhere else in the world (DOC,