Industrial development as a key factor explaining variances in soil and grass phyllosphere microbiomes in urban green spaces

https://doi.org/10.1016/j.envpol.2020.114201Get rights and content

Highlights

  • Urbanization might differently impact soil and grass phyllosphere microbial communities in urban green spaces.

  • Industrial development was a key driver shaping the bacterial community profiles in urban green spaces.

  • The impact of urbanization on the bacterial communities might derive from increased environmental pollution.

Abstract

Microbiota in urban green spaces underpin ecosystem services that are essential to environmental health and human wellbeing. However, the factors shaping the microbial communities in urban green spaces, especially those associated with turf grass phyllosphere, remain poorly understood. The lack of this knowledge greatly limits our ability to assess ecological, social and recreational benefits of urban green spaces in the context of global urbanization. In this study, we used amplicon sequencing to characterize soil and grass phyllosphere bacterial communities in 40 urban green spaces and three minimally disturbed national parks in Victoria, Australia. The results indicated that urbanization might have shown different impacts on soil and grass phyllosphere microbial communities. The bacterial diversity in soil but not in grass phyllosphere was significantly higher in urban green spaces than in national parks. Principal coordinate analysis revealed significant differences in the overall patterns of bacterial community composition between urban green spaces and national parks for both soil and grass phyllosphere. Industrial development, as represented by the number of industries in the region, was identified as a key driver shaping the bacterial community profiles in urban green spaces. Variation partitioning analysis suggested that industrial factors together with their interaction with other factors explained 20% and 28% of the variances in soil and grass phyllosphere bacterial communities, respectively. The findings highlight the importance of industrial development in driving the spatial patterns of urban microbiomes, and have important implication for the management of microbiomes in urban green spaces.

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).

References (75)

  • K.C. Jones et al.

    Persistent organic pollutants (POPs): state of the science

    Environ. Pollut.

    (1999)
  • N. Kabisch

    Ecosystem service implementation and governance challenges in urban green space planning—the case of Berlin, Germany

    Land Use Pol.

    (2015)
  • J. Klánová et al.

    Persistent organic pollutants in soils and sediments from James Ross Island, Antarctica

    Environ. Pollut.

    (2008)
  • W. Liang et al.

    Urbanization, economic growth and environmental pollution: evidence from China

    Sustain. Comput-Infor.

    (2019)
  • M. Manz et al.

    Persistent organic pollutants in agricultural soils of central Germany

    Sci. Total Environ.

    (2001)
  • G. Mhuireach et al.

    Urban greenness influences airborne bacterial community composition

    Sci. Total Environ.

    (2016)
  • J. Peñuelas et al.

    The foliar microbiome

    Trends Plant Sci.

    (2014)
  • S.T. Pickett et al.

    Urban ecological systems: Scientific foundations and a decade of progress

    J. EnviroN. Manage.

    (2011)
  • B.J. Reid et al.

    Bioavailability of persistent organic pollutants in soils and sediments—a perspective on mechanisms, consequences and assessment

    Environ. Pollut.

    (2000)
  • M.W. Strohbach et al.

    Above-ground carbon storage by urban trees in Leipzig, Germany: analysis of patterns in a European city

    Landsc. Urban Plann.

    (2012)
  • X. Wang et al.

    Composition and functional genes analysis of bacterial communities from urban parks of Shanghai, China and their role in ecosystem functionality

    Landsc. Urban Plann.

    (2018)
  • Z.Z. Yan et al.

    Antibiotic resistance in urban green spaces mirror the pattern of industrial distribution

    Environ. Int.

    (2019)
  • Australian Statistical Geography Standard (ASGS): volume 1 - main structure and greater capital city statistical areas, July 2016

  • Regional population growth, Australia, 2017-2018

  • H. Babich et al.

    Air pollution and microbial ecology

    Crit. Rev. Environ. Sci. Technol.

    (1974)
  • M.L. Cadenasso et al.

    Spatial heterogeneity in urban ecosystems: reconceptualizing land cover and a framework for classification

    Front. Ecol. Environ.

    (2007)
  • A. Canto et al.

    Micro-organisms behind the pollination scenes: microbial imprint on floral nectar sugar variation in a tropical plant community

    Ann. Bot.

    (2012)
  • J.G. Caporaso et al.

    QIIME allows analysis of high-throughput community sequencing data

    Nat. Methods

    (2010)
  • A. Chauhan et al.

    Assessment of ambient air quality status in urbanization, industrialization and commercial centers of Uttarakhand (India)

    N.Y. Sci. J.

    (2010)
  • H. Chen et al.

    VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R

    BMC Bioinf.

    (2011)
  • V. Cordovez et al.

    Ecology and evolution of plant microbiomes

    Annu. Rev. Microbiol.

    (2019)
  • T.W. Crowther et al.

    The global soil community and its influence on biogeochemistry

    Science

    (2019)
  • M.W. Dees et al.

    Bacterial communities associated with surfaces of leafy greens: shift in composition and decrease in richness over time

    Appl. Environ. Microbiol.

    (2015)
  • N. Delmotte et al.

    Community proteogenomics reveals insights into the physiology of phyllosphere bacteria

    Proc. Natl. Acad. Sci. U.S.A.

    (2009)
  • K.M. Docherty et al.

    Distributing regionally, distinguishing locally: examining the underlying effects of local land use on airborne bacterial biodiversity

    Environ. Microbiol.

    (2018)
  • R.C. Edgar

    Search and clustering orders of magnitude faster than BLAST

    Bioinformatics

    (2010)
  • D.J. Eldridge et al.

    Grazing regulates the spatial heterogeneity of soil microbial communities within ecological networks

    Ecosystems

    (2019)
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