Impact of Human Disturbances on Soil Cyanobacteria Diversity and Distribution in Suburban Arid Area of Marrakesh, Morocco Z
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Hakkoum et al. Ecological Processes (2021) 10:42 https://doi.org/10.1186/s13717-021-00303-7 RESEARCH Open Access Impact of human disturbances on soil cyanobacteria diversity and distribution in suburban arid area of Marrakesh, Morocco Z. Hakkoum1, F. Minaoui1, M. Douma1,2, K. Mouhri1 and M. Loudiki1* Abstract Background: Cyanobacteria are among the first photoautotrophic component of soil microorganism communities which play a key ecological role in nutrient cycles and soil productivity. However, the sustainability of these soil biodiversity ecosystem services is increasingly compromised, especially in urban and peri-urban areas where soils are heavily exploited and used for a wide range of human activities. The aim of this study is to assess the impact of different types of human disturbances on cyanobacteria diversity and distribution in suburban soils of Marrakesh. Soil and cyanobacteria sampling were carried out during two campaigns at six sites located along an anthropogenic gradient from the least urbanized suburbs of Marrakesh to the highly anthropized suburban area. In the laboratory, soil physicochemical characteristics were measured. The morphological identification of cyanobacteria species was based both on microscopic observation and on soil cultures in solid and liquid Z8 media. Results: The results showed a total of 25 cyanobacteria taxa belonging to ten genera, four families, and two orders (Oscillatoriales 88% and Chroococcales 12% of taxa). Among the taxa identified, seven strains were isolated in soil culture in nutrient media and purified in monoalgal culture. The highest cyanobacterial diversity was recorded in irrigated soil with treated wastewater compared to the non-cultivated control soil. In Principal Component and Cluster Analysis, suburban soils were subdivided into three groups depending on the chemical properties and cyanobacteria composition. Cyanobacteria diversity was significantly associated with the soil moisture, total organic carbon (TOC), PO4-P, NO3-N, and NH4-N contents. Conclusions: While diversity and microalgal biomass were significantly lower in the soils affected by municipal and mining solid wastes, the input of organic matter and nutrients from treated wastewater appears to be beneficial for the increasing of the biodiversity of soil cyanobacteria. This survey provides a first inventory of the soil cyanobacterial communities and shows their spatial variability and high sensitivity to the land-use practices and anthropogenic disturbances on urban soil in Moroccan drylands. Keywords: Cyanobacteria, Peri-urban soils, Pollution, Anthropogenic effects, Moroccan drylands * Correspondence: [email protected] 1Laboratory of Water, Biodiversity and Climate Change; Phycology, Biotechnology and Environmental Toxicology Research Unit, Faculty of Sciences Semlalia Marrakesh, Cadi Ayyad University, Av. Prince My Abdellah, P.O. Box 2390, 40000 Marrakesh, Morocco Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. Hakkoum et al. Ecological Processes (2021) 10:42 Page 2 of 16 Introduction disturbance and cause considerable harm to vegetation Cyanobacteria are the oldest photoautotrophic component and soil microorganisms (El Alaoui et al. 2019). of microbiota that include archaea, bacteria, microalgae, Soil is a complex environment characterized by a wide microfungi, lichens, and protozoa ( Rivera-Aguilar et al. variety of microorganisms, chemical compounds, and 2006; Maestre et al. 2011). They are a diverse group of complex physical structure. It not only ensures terrestrial prokaryotes found in a wide array of aquatic and terres- biodiversity, but also provides habitat for a large number trial habitats and are well adapted to hostile environments of organisms (Bardgett et al. 2005; Briones 2014). Urban like extremely arid and dryland areas (Douma 2010). soils and their biodiversity provide a variety of ecosystem Thanks to their numerous adaptations, they can colonize services, including nutrient cycling, depollution, fertility, unstable substrates and their presence can also improve and carbon storage (Guilland et al. 2018). However, these the environmental role and functions of the soil biocrust urban soil biodiversity functions are threatened by through carbon sequestration and nitrogen fixation (Büdel urbanization, compaction, and pollution which cause ac- et al. 2016). They are pioneers on many nutrient-poor and cumulation of various contaminants, chemical compounds abiotically stressful substrates, creating stable organo- and heavy metals, changes in humus content, organic car- mineral layers on which other species can subsequently bon, and pH (Carrino-Kyker et al. 2011; Maltsev et al. recruit and grow (Rossi and De Philippis 2015). Cyanobac- 2017;Lietal.2017). Urbanization processes in natural teria are well known for their agronomic importance, act- landscapes have caused some changes in the biological ing as one of the major determinants of soil fertility by factor of soil formation and the creation of artificial eco- adding organic matter, nitrogen and phosphorus (Whitton logical systems (Rai et al. 2018;Wangetal.2020). and Potts 2007; Singh et al. 2014; Rossi et al. 2017), redu- Urbanization also results in the creation of specific bio- cing the erosion of soil and thus favoring the settlement of topes with a species composition characteristic of living vascular plants (Lin et al. 2013). They may also contribute organisms (Caruso et al. 2017;Joimeletal.2017). This soil to the suppression of phytopathogens (Prasanna et al. habitats alteration is drastic and is increasing at an alarm- 2013) and produce substances (phytohormones, carbonic ing rate, and has emerged as a major threat to the soil acids, polysaccharides) that promote plant growth (Rodrí- microbial biodiversity (McKinney 2006). Although the re- guez et al. 2006; Karthikeyan et al. 2007; Shariatmadari search on soil biodiversity has grown exponentially over et al. 2013) and improve soil aggregation and structural the last two decades, work has been concentrated on stability (Song et al. 2005). Moreover, cyanobacteria are natural environments and few investigations have been best known for their adaptability to survive in polluted carried out on urban soils (Joimel et al. 2017;Guilland and heavily polluted environments and their capacity to et al. 2018; Rutgers et al. 2019). More recently, the investi- degrade organic waste, various agrochemicals (pesticides, gation of microbial biodiversity in urban ecosystems has herbicides) and remove heavy metals and other pollutants gained interest as an important feature of ecological inves- (Vijayakumar 2012; Subashchandrabose et al. 2013;Singh tigations. Prokaryotic microalgae are an indispensable part et al. 2014). of soil biodiversity and urban ecosystems, performing an Although several recent researches have shown the important regulatory function and play a key role as pri- ecological functions and great biotechnological potential mary producers, in self-purification processes and support of cyanobacteria as bio-resource in agriculture, soil eco- the ecological stability (Shekhovtseva 2014; Maltsev et al. system remediation, and environmental sustainability 2017). Other researchers suggest that their high sensitivity (Singh et al. 2016; Bag et al. 2019; Rocha et al. 2020), the to environmental stressors and their omnipresence and ecosystem services of cyanobacterial soil diversity are short generation time also highlight their potential as threatened by urban, agricultural and industrial land bioindicators of global change (Kannan et al. 2012; uses. Indeed, the advancing urbanization and the in- Muñoz-Martín et al. 2019). Indeed, cyanobacteria and crease of domestic and agro-industrial effluents and eukaryotic microalgae (notably diatoms) have been wastes have caused the deterioration of soil microbial used as bioindicators of soil health in ecological mon- communities, including cyanobacteria (Sharma 2015). itoring (Maltsev et al. 2017;Barragánetal.2017; The agricultural activities are places of intensive an- Foets et al. 2021). thropogenic activity, including tillage and the application Reports on terrestrial algal communities including of chemical fertilizers, pesticides, and herbicides. Such cyanobacteria in urban habitats have gradually emerged human activities affect the physicochemical properties of in the last two decades (Rindi and Guiry 2019; Doro- soils and thus could reduce the diversity of soil microal- khova et al. 2015; Maltsev et al. 2017; Rai et al. 2018). gae, including cyanobacteria (Mostafa and Helling 2002). Most of these studies were carried out in European, Furthermore, mining activities