Industrial development as a key factor explaining variances in soil and grass phyllosphere microbiomes in urban green spaces☆
Graphical abstract
Introduction
Microorganisms, as a vital component of the urban ecosystem, play a critical role in regulating ecosystem services (Eldridge et al., 2019; Hui et al., 2017; Kabisch, 2015), such as pollutant remediation, nutrient cycling and genetic diversity preservation (Escobedo et al., 2011; Groffman et al., 2009; Ramirez et al., 2014, Strohbach and HAASE, 2012). These ecosystem functions are important in reducing the growing global burden of urban-associated chronic diseases and maintaining the wellbeing of urban environment and city dwellers. There has been evidence that exposure of humans to microorganisms associated with soil and plants in urban green spaces could reduce the dysfunction of immune system and supress inflammation (Flies et al., 2017; Flies et al., 2018). During the past several decades, the massive transition of human population from rural to urban living has resulted in dramatic alternations of land use types which may consequently change the environmental habitats for microorganisms (Grimm et al., 2008; Li et al., 2018; Zhu et al., 2011). A better understanding of how anthropogenic disturbance impacts microbial community profiles in the urban environment is essential to prediction and mitigation of the influence of urbanization on ecosystem functioning (Falkowski et al., 2008; Kaye et al., 2005; Reese et al., 2016).
Soil and the aerial part (phyllosphere) of turf grass are the two largest habitats for microorganisms in urban green spaces (Crowther et al., 2019; Lindow and Brandl, 2003; Peñuelas and Terradas, 2014; Vorholt, 2012). Urban ecosystem is subject to intensive management practices, and therefore the microbial communities in urban green spaces are not only influenced by environmental factors (e.g. soil properties and climate factors) (Hui et al., 2017; Wang et al., 2018a) but also by anthropogenic activities. Urban environment is considered as a social economic ecosystem (Cadenasso et al., 2007; Pickett et al., 2011) characterized by high human population density and rapid economic growth (Wang et al., 2018a; Zhu et al., 2017). The increasing demand for material by a growing population is usually associated with urban expansion, resulting in an increasing number of industries in the region, which is considered as another important measurement of urbanization (Xu et al., 2014). To date, a few studies have reported that urbanization can substantially change the microbiota in urban green spaces (Francini et al., 2018; Hui et al., 2017; Ramirez et al., 2014; Wang et al., 2018a; Xu et al., 2014), but it remains largely unknown which aspects of urbanization account for the major variance in microbial community profiles in urban green spaces. Additionally, previous studies have mostly focused on the impact of urbanization on soil microbiota but overlooked the plant phyllosphere microbiota despite the significance of phyllosphere as an important environmental habitat for microorganisms. As a vast environment with an estimated area of >1 billion km2 across the globe (Vorholt, 2012; Woodward and Lomas, 2004), phyllosphere is described as a formidable playground for testing fundamental ecological principles in microbiology (Meyer and Leveau, 2012). In addition to promoting plant growth and production (Canto and Herrera, 2012; Grady et al., 2019; Taghavi et al., 2009), phyllosphere microbiomes have other important ecosystem functions, for example participating in Earth’s biogeochemical cycles through moderating plant ethanol emission and contributing to nitrogen fixation (Galbally and Kirstine, 2002; Fürnkranz et al., 2008). In addition, phyllosphere microbiomes are closely linked to human health as phyllosphere is the potential bridge between environmental microbiome and human microbiome (Chen et al., 2018).
In this study, we used Illumina Miseq sequencing to analyse microbial communities in soil and grass phyllosphere samples collected from 40 urban green spaces across the Greater Melbourne metropolitan. As the capital of Australian state Victoria and the second most populous city in Oceania (ABS, 2019), Melbourne is a highly urbanized city with a long legacy of public green space development. In addition, samples from three national parks from remote Victoria were studied as representative of environments with minimal anthropogenic disturbance. Multiple factors including soil properties and anthropogenic parameters were collected to interpret their impacts on the microbial community profiles in urban green spaces. The main aims of this study were to (i) determine the potential differences and links between soil and grass phyllosphere bacterial communities; (ii) compare the bacterial community profiles in highly urbanized environment with those in minimally disturbed natural environment; and (iii) determine the most important factors shaping the bacterial community profiles in urban green spaces.
Section snippets
Sampling
Soil and grass samples were collected during May 2018 from 40 urban parks across Greater Melbourne metropolitan and three national parks in remote Victoria, Australia. All samples were collected on sunny or cloudy days with no rainfall event. The daytime temperature during the sample collection period ranged from 12.6 °C to 19.5 °C. At each park, three independent samples for each sample type (i.e. soil and grass) were collected. The surface 5 cm of soil and aerial parts of grass were
Soil properties
Three independent soil samples were collected from each of the 40 urban green spaces. In total, 120 soil samples were characterized for physiochemical properties. The soil properties, including soil pH, EC (ds m−1), CEC (com kg−1), TC (%), TN (%), ammonium (mg L−1) and nitrate (mg L−1) contents are summarised in Table S3. Soil pH ranged from 5.56 to 7.98, and more than 80% of the soils had pH values below 7. Only 23 soil samples were alkalescent or alkaline. Soil EC ranged from 0.06 (ds m−1) to
Distinct responses of soil and grass phyllosphere bacterial communities to urbanization
The impact of urbanization on microbial diversity has received substantial attention, because loss of microbial diversity could potentially lead to serious environmental and human health problems (Philippot et al., 2013; Rook, 2009; Wang et al., 2018b). The significantly higher soil bacterial α diversity in urban green spaces than in national parks (Fig. S4A) indicated that urbanization might lead to an increase in soil bacterial diversity. Other studies of soil microbial diversity in parks of
Conclusions
In this study, we comprehensively characterized the soil and grass phyllosphere bacterial communities in urban green spaces. Our findings indicated that urbanization could have altered bacterial community profiles, and the alternations were different for below ground (soil) and above ground (grass phyllosphere) microbiomes. Most importantly, we found that compared with soil properties, anthropogenic changes, particularly industrial development may play a more significant role in shaping
CRediT authorship contribution statement
Zhen-Zhen Yan: Data curation, Methodology, Formal analysis, Writing - original draft. Qing-Lin Chen: Methodology, Writing - review & editing. Yu-Jing Zhang: Writing - review & editing. Ji-Zheng He: Writing - review & editing, Funding acquisition, Project administration. Hang-Wei Hu: Writing - review & editing, Funding acquisition, Project administration.
Declaration of competing interest
The authors declare no conflict of interest.
Acknowledgements
This work was financially supported by Australian Research Council (DP170103628).
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This paper has been recommended for acceptance by Klaus Kümmerer.