Interactions of soil metals with glomalin-related soil protein as soil pollution bioindicators in mangrove wetland ecosystems

Highlights

• Revealing soil pollution by combining GRSP traits with multivariate analysis.

• Soil environment process had no effect on the type of functional groups of GRSP.

• Molecular composition ratios of GRSP were field-specific in mangrove soils.

• GRSP-bound metals were linked with metal pollution sources in coastal wetlands.

• GRSP, a novel bioindicator, provided new perspective for coastal management.

Abstract

Through binding of mineral particles and elements, glomalin-related soil protein (GRSP) plays a critical role in sustaining terrestrial soil quality and contributes to the fate of elements from terrestrial to aquatic ecosystems. There is little knowledge, however, of the metal sequestration patterns of GRSP in both terrestrial and aquatic soils, and this limits progress in understanding how environmental conditions influence GRSP characteristics. Here, we employed microcosm experiments to determine the molecular composition of original GRSP derived from three arbuscular mycorrhizal fungi, Glomus intraradices, Glomus versiforme and Acaulospora laevis. To gain insight into the metal sequestration patterns of environmental GRSP, we investigated major subtropical and tropical mangrove wetlands in southern China. GRSP-bound metals were significantly and positively correlated with total metals, and the metal binding contributed to the metal sequestration of mangrove soils. Fourier-transform infrared spectroscopy results showed that original- and environmental GRSP fractions contained hydroxyl, carboxyl, amide and carbonyl functional groups, which enhanced metal binding. Environmental process had no effect on the type of functional groups of the GRSP, while it significantly changed the relative content of the functional groups. The infrared fingerprint analyses of original- and environmental GRSP revealed field-specific, however, no taxon-specific characteristics of GRSP. Biostatistical analysis of the GRSP molecular composition further revealed that the soil pollution sources regulated the ratios of functional group contents associated with hydrocarbons, proteins, polysaccharides and nucleic acids. By GRSP infrared fingerprints coupled with multivariate analyses, we developed a technique for source identification of heavy metal pollution, giving more reliable evidence about contributing sources.

Introduction

Arbuscular mycorrhizal (AM) fungi form mutualistic associations with the roots of >80% of land plants on earth (Smith and Read, 2010), which increases stabilization or removal of heavy metals, and plays a crucial role in soil environmental processes (Ma et al., 2019). Those ecological roles of AM fungi are in fact linked with the production of a novel AM-fungal substance, glomalin-related soil protein (GRSP), which is an operationally defined heterogenous organic fraction (Rillig, 2004; Wright and Upadhyaya, 1998). GRSP has been described within mycorrhizal fungal cell walls, and accumulates in soil after the fungal hyphae senesce and decompose (Driver et al., 2005), and further contributes to soil metal binding and stabilization (Gonzalez-Chavez et al., 2004).

GRSP possesses a high binding capacity for metals such as Cu and Cd (Cornejo et al., 2008; Gonzalez-Chavez et al., 2004; Jia et al., 2016); while GRSP and associated metals can be transported by soil erosion and river, and it is deposited in floodplain soils, accretion areas and coastal systems (Adame et al., 2012; Chern et al., 2007; Harner et al., 2004). GRSP is transported to the coastal anoxic environments where it accumulates and remains non-degraded, enabling the assessment of its potential as a palaeoecological proxy for soil organic matter accrual and ecosystem health (López-Merino et al., 2015). Thus, further description of the characteristics of GRSP fraction in the terrestrial-aquatic environment can provide new information on its importance as a sink and source of metals in coastal wetland ecosystem (Adame et al., 2010; Adame et al., 2012; Wang et al., 2018a).

Mangrove wetlands along coastlines throughout the tropics and subtropics are a key ecological buffer zone that links terrestrial and marine environments (Bouillon et al., 2008; Rovai et al., 2018). Multi-source heavy metals including agricultural, industrial and natural origins are ultimately discharged by soil erosion and runoff from land into the coastal mangrove wetland, causing significant pollution and degradation (Wang et al., 2013). Thus it is crucial to identify the sources of heavy metals in coastal wetland for designing pollution controls and remediation strategies. Multivariate analyses such as principal component analysis, the non-metric multidimensional scaling and cluster analysis are valuable tools for identifying sources of heavy metals in soil (Ma et al., 2016). These procedures, coupled with bioindicators, are proven to be more accurate to identify the pollution source (Dragovic and Mihailovic, 2009). Previous studies demonstrated that GRSP can be used as a bioindicator of terrestrial-marine linkages and soil quality (Adame et al., 2012), and is an important carrier for metal loading in coastal wetland soils (Chern et al., 2007) and form a potential depositional store (Wang et al., 2018b; Wang et al., 2019a). However, there is no known knowledge in whether GRSP fraction can be used as a bioindicator of soil metal pollution when GRSP and associated metals are transported into coastal wetlands. The proportion of GRSP in fungal hyphae can be affected by environmental factors (Rillig and Steinberg, 2002) and can vary among fungal species and isolates (Wright and Upadhyaya, 1996). However, current studies have not revealed the chemical components of GRSP produced from different AM fungi, whether its chemical components have environmental specific features and whether GRSP can serve as a bioindicator of soil pollution source identification.

The overall objective was to combine the microcosm experiment with large-scale field investigation to comprehensively assess GRSP as a bioindicator for metal pollution in mangrove soils. Specifically, the present study aimed to: (i) characterize the molecular components of the original GRSP and the environmental GRSP and to further identify and classify pollution sources at large-scale mangrove areas; (ii) analyze the metal sequestration capacities and contributions of GRSP and its interaction with the mangrove soil environment; (iii) explore the response and feedback of GRSP-bound metals to mangrove soil pollution.