Native plant Maireana brevifolia drives prokaryotic microbial community development in alkaline Fe ore tailings under semi-arid climatic conditions

https://doi.org/10.1016/j.scitotenv.2020.144019Get rights and content

Highlights

  • Prokaryotic microbial community in alkaline Fe-ore tailings was addressed.

  • Tailings are dominant in microbes with alkaline tolerance and Fe redox capacity.

  • Maireana brevifolia colonisation increased prokaryotic microbial abundance and diversity.

  • M. brevifolia favoured bacteria related to N cycling and OM degradation.

  • M. brevifolia could be integrated into eco-engineering tailings-soil formation.

Abstract

Native pioneer plants of high environmental tolerance may be exploited as early colonisers in alkaline Fe-ore tailings to drive the development of functional prokaryotic microbial communities, which is one of the critical pedogenic processes leading to in situ soil formation in the tailings. The present study deployed high throughput Illumina Miseq sequencing, to characterise the diversity and potential functionality of prokaryotic microbial communities in the aged Fe-ore tailings and topsoils colonised by native plant species Maireana brevifolia at an Fe ore mine in Western Australia, in comparison with those in the tailings/topsoils without plants. The composition of prokaryotic microbial communities differed between the aged tailings (AT) and topsoil sites (TS). Aged tailings (AT1-AT3) contained more bacteria tolerant of alkaline/saline conditions (e.g., Alkalilimnicola sp.) and those related to Fe biogeochemical cycling (e.g., Acidiferrobacter sp., Aciditerrimonas sp.). In comparison, the prokaryotic microbial communities in the topsoil (TS) contained abundant bacteria related to N cycling (e.g., Rhizobium sp., Frankia sp.). The presence of M. brevifolia plants significantly increased the diversity of prokaryotic microbial communities in tailings and topsoil, particularly favouring the development of bacteria related to N cycling and OM degradations (e.g., Mesorhizobium sp. Paracoccus sp., Oxalicibacterium horti, and Microbacterium sp.). The variation of microbial community were mainly explained by pH, amorphous Fe, and total N, which were regulated by M. brevifolia colonisation. The beneficial roles of pioneer plants M. brevifolia in the development of prokaryotic microbial community in the alkaline Fe ore tailings may be integrated as a key factor when designing and scaling up the process of eco-engineering Fe-ore tailings into soil under semi-arid climatic conditions.

Introduction

Eco-engineering tailings into soil-like growth media (i.e., technosol) has been advocated as a promising technology for cost-effective and sustainable rehabilitation of Fe-ore tailings without requirements for large volumes of natural topsoil. In this process, functional microbes and pioneer plants were important factors in driving mineral weathering, organic matter sequestration and soil structure development (Huang et al., 2014; Wu et al., 2019a). Tolerant microorganisms are usually pioneers initially colonizing the tailings of unfavourable conditions, with the capability to drive nutrient cycling in tailings (de Zelicourt et al., 2013). Some lithotrophic microbes such as Fe oxidizing/reducing bacteria, are involved in mineral weathering and secondary mineral formation (Chan et al., 2011), leading to physicochemical and mineralogical improvement in the tailings (Huang et al., 2012). Prokaryotic microbial communities of low diversity are found in metal mine tailings, for example, Proteobacteria (belongs to Bacteria) and Euryarchaeota (especially Ferroplasma sp., belongs to Archaea) as dominant groups in an acid lead/zinc tailings (Chen et al., 2013), and Truepera, Thiobacillus, and Rubrobacter as dominant extremophiles and lithotrophs in an circumneutral sulfidic tailings (Li et al., 2015). In acidic copper mine tailings, Proteobacteria and Actinobacteria were found to be rich in the revegetated area (Wu et al., 2018). However, little has been known about the microbial diversity and community in alkaline metal mine tailings undergoing natural weathering under field conditions, such as magnetite Fe ore tailings, which had initial alkaline pH (9.5–10) condition and extremely low organic matter and nitrogen (Wu et al., 2019b, Wu et al., 2019c).

Native pioneer plants may be exploited to provide rhizosphere moisture and organic substrates to support the growth and functions of diverse microbial species under semi-arid climatic conditions (Burns et al., 2015; Sasse et al., 2018; Zhalnina et al., 2018; Zipfel and Oldroyd, 2017). Many Australian native plants are indigenous to semi-arid landscapes and highly tolerant of drought, salinity, and poor nutrient availability in soil, such as Acacia spp. (e.g., A. sibina, A. ramulosa), Eucalyptus spp. (e.g., E. leptopoda, E. kochii), Melaleuca leiocarpa, Allocasuarina acutivalvis, Callitris columellaris, and Maireana brevifolia (Markey and Dillon, 2008; You et al., 2016). Particularly, the role of pioneer plants in hosting microbial community becomes much important when short-term irrigation to cover thousands of hectare of tailings landscapes is not feasible at remote mine sites. The diversity and abundance of microbial communities in tailings may be enhanced with pH neutralization and increasing organic matter from natural and/or artificial sources, in response to plant colonisation over time. For example, in sulfidic tailings, plant colonisation tended to shift the bacterial community structure from autotroph-dominant to heterotroph-dominant communities (Li et al., 2015). The relative abundance of Leptospirillum and Acidithiobacillus (Fe- and S-oxidizing bacteria) declined in response to plant colonisation in the sulfidic tailings (Li et al., 2016). Yang et al. (2017) found that plant colonisation enhanced the dominance of Proteobacteria, rather than Euryarchaeota, Ferroplasma and Aplasma, in an extremely acidic Cu mine tailings. As a result, tolerant and native plant may be introduced to shape bacterial community composition and increase the diversity in tailings. These microbial responses to plant colonisation would induce changes in microbial functionalities and associated biogeochemical and pedogenic processes.

In a previous study, we found a native pioneer plant species Maireana brevifolia, which naturally colonised aged alkaline Fe ore tailings without any significant amendments at the edge of tailings landscapes, under semi-arid climatic conditions (Wu et al., 2019b). Therefore, it is expected that the colonisation of this plant species would host diverse functional groups of prokaryotic microbes in the basal area (including rhizosphere and litter-impacted surface area below canopy), with potential functions in stimulating mineral weathering and soil formation in the tailings, such as biogeochemical cycling of Fe and N. The present study thus aimed to characterise prokaryotic microbial diversity and community across tailings and topsoil sites, in response to the natural colonisation of Maireana brevifolia plants under semi-arid climatic conditions at a magnetite Fe-ore mine, Western Australia.

A systematic sampling was carried out by sampling paired sites with/without the pioneer plants, across an area of aged tailings (without any topsoil cover), in comparison with an adjacent area covered by natural topsoil (about 30 cm thick). By deploying the latest high throughput 16S rRNA gene sequencing technique, specific questions were addressed, including: (1) what are dominant groups of prokaryotic microbes in the alkaline Fe ore tailings, compared to those in topsoils? (2) whether pioneer plant M. brevifolia colonisation could induce changes in the diversity and dominant groups of prokaryotic microbial community in the tailings and topsoils? It is expected that the colonisation of M. brevifolia could help increase microbial diversity and shift microbial community structure in the aged tailings away from the prokaryotic microbial community composition dominated by a small number of extremely tolerant microbes typical of the extreme tailing environment.

Section snippets

Field description and sampling

The tailings and topsoil samples were systematically collected at sites colonised by the same native plant species Maireana brevifolia, at a magnetite Fe ore tailing dam, under Mediterranean semi-arid climatic conditions in Western Australia (Wu et al., 2019b). A total of 5 sites were sampled, representing different domains of the tailings landscape (Fig. 1). These included one fresh tailing site (FT, less than 2 months), three aged tailing sites (AT1 in the top dam area, 2–3 years; AT2, in the

Physicochemical properties of tailings across the mine site

Generally, the physicochemical properties of the tailings were significantly different from those in the topsoil. Fresh (FT) and aged tailings (AT1-AT3) generally had higher EC, but lower levels of TOC and TN, than the topsoil covering the tailings (TS) (Table 1). The FT and AT tailings samples contained more AAO-extractable Fe but less Al, than the TS samples. The levels of AAO-Si, K, Mg in AT1 sites were generally higher than those of other sites (Table 1).

In the AT3 and TS samples, plant

Discussion

Prokaryotic microbial communities in the Fe-ore tailings tended to increase slowly in diversity and abundance of functional groups as the tailings naturally aged under field conditions (i.e., semiarid Mediterranean climatic conditions), without any ecological engineering inputs. Despite several years of aging under field conditions, microbial communities in the tailings remained low in diversity, with dominant groups typical of alkaline/saline tolerance and Fe/S redox capacity. As expected, the

Conclusions

Overall, the present study revealed the microbial shifts from those with tolerant of alkaline/saline conditions to those related to N cycling and organic matter degradation, in alkaline Fe-ore tailings and topsoil sites at a Fe-ore mine under semi-arid climatic conditions. The native and drought tolerant pioneer plant species M. brevifolia naturally colonised the aged and alkaline Fe ore tailings under Mediterranean and semi-arid climatic conditions, without any management inputs. The presence

CRediT authorship contribution statement

Songlin Wu: Conceptualization, Investigation, Methodology, Formal analysis, Data curation, Writing – original draft. Fang You: Methodology, Software, Formal analysis, Writing – review & editing. Merinda Hall: Investigation, Writing – review & editing. Longbin Huang: Supervision, Conceptualization, Project administration, Funding acquisition, Writing – review & editing.

Declaration of competing interest

The authors of the above manuscript certify that they have NO conflict of interest regarding this manuscript.

Acknowledgement

The work is financially supported by Australia Research Council Linkage Project (LP160100598), Karara Mining Limited, and The Botanic Gardens and Parks Authority (BGPA). The authors also thank the Australian Centre for Ecogenomics, the University of Queensland, Australia for Illumina sequencing analysis. Mr. T. Chiu was acknowledged for help on DNA extraction. We also acknowledge Dr. Jun Ye and Dr. Zhaoxiang Wu for help on the improvement of the manuscript.

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    Songlin Wu and Fang You contribute equally to the current study.

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