Plant growth and arbuscular mycorrhizae development

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Plant growth was reduced in oil sands processing by-product substrates.
• AMF colonization of Elymus trachycaulus was not influenced by soil hydrocarbons.
• AMF colonization of Lotus corniculatus without bacteria decreased in coarse
• Mycorrhizae plus bacteria inoculation improved plant growth in coarse tailings
• Soil bacteria increased root branching in coarse tailings sand and tailings mix.

pot stand| plant pot stand| timber plant stand




Soil pollutants such as hydrocarbons can induce toxic effects in plants and associated arbuscular mycorrhizal tall pot plant stand fungi (AMF). This study was conducted to evaluate if the legume Lotus corniculatus and the grass Elymus
trachycaulus and arbuscular mycorrhizal fungi could grow in two oil sands processing by-products after bitumen
extraction from the oil sands in northern Alberta, Canada. Substrate treatments were coarse tailings sand (CTS), a
mix of dry mature fine tailings (MFT) with CTS (1:1) and Pleistocene sandy soil (hydrocarbon free); microbial , tall pot plant stand treatments were without AMF, with AMF and AMF plus soil bacteria isolated from oil sands reclamation sites.
Plant biomass, root morphology, leaf water content, shoot tissue phosphorus content and mycorrhizal colonization
were evaluated. Both plant species had reduced growth in CTS and tailings mix relative to sandy soil. AMF
frequency and intensity in roots of E. trachycaulus was not influenced by soil hydrocarbons; however, it decreased
significantly over time in roots of L. corniculatus without bacteria in CTS. Mycorrhizal inoculation alone did not
significantly improve plant growth in CTS and tailings mix; however, inoculation with mycorrhizae plus bacteria
led to a significantly positive response of both plant species in CTS. Thus, combined inoculation with selected mycorrhizae
and bacteria led to synergistic effects. Such combinations may be used in future to improve plant, plant stands, plant shelf growth in the reclamation of CTS and tailings mix.

Soil and biotic factors, such as those induced from soil pollutants like
heavy metals, hydrocarbons and other industrial chemicals, influence
Science of the Total Environment 621 (2018) 30–39
⁎ Corresponding author at: Brandenburg University of Technology Cottbus-Senftenberg,
Chair of Soil Protection and Recultivation, Konrad-Wachsmann-Allee 6, D-03046 Cottbus,
E-mail address: (K. Boldt-Burisch).
0048-9697/© 2017 Elsevier B.V. All rights reserved.
Contents lists available at ScienceDirect Science of the Total Environment
journal homepage: plant physiological and ecological responses to environmental stress (Orcutt and Nilsen, 2000). Bitumen extraction from the oil sands in
northern Alberta, Canada, results in large areas of disturbed land and
large amounts of by-products, known as tailings. Tailings contain a mixture
of water, clay, un-recovered bitumen, solvent and dissolved
chemicals, including some organic compounds (Natural Resources
Canada, 2013). The presence of naphthenic acids in oil sands tailings
has led to environmental and industrial concerns, as they are known
to be toxic to aquatic organisms, algae and mammals (Mohamed et al.,
Tailings are stored in large ponds similar to water dams. The water
released from the ponds can be recycled and reused in oil sands processing,
however, the majority has historically remained as mud and has to
be stored long term. Due to settling processes in tailing ponds, different
fractions of tailings including coarse tailings sands (CTS) and mature
fine tailings (MFT) can be obtained. Those materials still contain
residual hydrocarbons (Lefrancois et al., 2010). These hydrocarbons
can increase stress levels for plants (Alkio et al., 2005). Dried MFT
(processed MFT treated with a flocculant for dewatering) contains significantly
more polycyclic aromatic hydrocarbons than coarse tailings
sands due to enrichment during the consolidation process (Noah et al.,
2014). Both materials are currently used for land reclamation; however,
knowledge of effects of these materials on plant growth, especially herbaceous
pioneer plants, is sparse. Environmental challenges associated
with oil sands mining continue to require improved reclamation activities
to address environmental sustainability and the reconstruction of
the disturbed landscapes.
Various studies were carried out on reclamation oil sands sites using
organic materials such as peat mineral mix and forest floor as a cover
(Brown and Naeth, 2014; Jamro et al., 2014; Kwak et al., 2015). Studies
of Adam and Duncan (1999) and Olson and Fletcher (2000) showed that
Bermuda grass (Cynodon dactylon L. (Pers.)), sunflower (Helianthus
annuus L.), southern crabgrass (Digitaria ciliaris (Retz.) Koeler) and red
clover (Trifolium pratense L.) are hydrocarbon tolerant plants (Kaimi
et al., 2007). Thus grasses and legumes could be useful for reclaiming
hydrocarbon polluted soils, although, less is known about the direct
interactions of plants and oil sands processing by-products.
Residual hydrocarbons in soil can influence plant, Timber Plant Stand development by inducing phytotoxic effects from volatile compounds and hydrophobicity (Kaimi et al., 2007; Alejandro-Cordova et al., 2017). Volatile hydrocarbons can easily move through cell membranes, causing toxic effects
(Adam and Duncan, 2002). Hydrophobicity of oil-contaminated soils
can prevent water infiltration and aeration, which may disrupt plant water
relations and plant metabolism (Racine, 1994; Kaimi et al.,
2007), reducing plant and shoot biomass and increasing carbohydrate
contents of plants (Rahbar et al., 2012). High concentrations of hydrocarbons
in soil can inhibit and limit microbial community biodiversity
(Alejandro-Cordova et al., 2017), such as arbuscular mycorrhizal fungi.
Over 80% of land plants live in a mutualistic relationship with AMF
(Smith and Read, 2010) and many of them are obligate dependents on
their symbiotic AMF partner. These fungi are known to improve plant
growth and vitality by enhancing nutrient supply and by increasing the
tolerance to abiotic and biotic stresses (Clark and Zeto, 2000; Turnau
and Haselwandter, 2002). Some oil sands processing by-products may
negatively influence AMF development and plant establishment due to
their high content and number of hydrocarbons. Gaspar et al. (2002),
Rabie (2005) and Wu et al. (2009) found that polycyclic aromatic compounds
(PAH) negatively affected AMF spore germination, extraradical
hyphae elongation, root colonization and sporulation, and thus may impact
successful and sustainable plant development. Mycorrhizal fungi
and bacteria in the rhizosphere can synergistically interact, through surface
attachment and intimate and tall pot plant stand obligatory symbiosis (Perotto and
Bonfante, 1997). This synergism may be important in promoting plant
growth and health in a hydrocarbon containing soils, since bacteria such
as plant growth-promoting rhizobacteria can support plant growth
directly by releasing phytohormones and antimicrobial compounds
against pathogens (Perotto and Bonfante, 1997) or indirectly by stimulating
the relationship between the host plant and mycorrhizal fungi
(Hrynkiewicz and Baum, 2011).
A greenhouse study was conducted to determine plant response to
two substrates of oil sands processing by-products in combination
with different microbial treatments.We hypothesized that AMF would
survive in oil sands processing by-products, that microbial additions
would stimulate mycorrhization, and that AMFplus bacteria inoculation
would have the most positive effect on plant growth. Grasses and legumes
with their very different root systems may have different relationships
with AMF and bacteria in oil sands processing by-products.
Thus, the legumeL. corniculatus and the grass E. trachycaulus, commonly
used species for reclamation of other materials in Alberta, were investigated.
Such information is important for utilization of substrates and
cover materials containing residual hydrocarbons in reclamation.
2. Material and methods
2.1. Substrate materials
Two oil sands processing by-products, coarse tailings sand (CTS) and
dry mature fine tailings (MFT), were provided by Shell Canada in Fort
McMurray (Alberta, Canada). A Pleistocene, calcareous, sandy overburden
substrate (sandy soil) was retrieved from the forefield of the open
cast lignite mining area atWelzow-Süd in Germany to serve as a reference
material with physical properties similar to those of CTS, butwithout
the influence of oil sands derived hydrocarbons. A detailed substrate
characterization for petroleum hydrocarbons and oil sands derived biomarkers
was conducted by Noah et al. (2014); oil sands derived
hopanes, steranes, monoaromatic and triaromatic steroids, PAHs and
dissolved inorganic and organic ions in pore water were analyzed in
all MFT and CTS from reclamation sites. In dried MFT mean concentration
of hopanes and tricyclic terpanes (aliphatic hydrocarbon fraction)
was 1182 ng/g sediment and for CTS 474 ng/g sediment. Aromatic hydrocarbonswere
significantly higher in driedMFT (365–1646 ng/g sediment)
then in CTS (below the detection limit of 97 ng/g sediment).
Mean chloride and sulfate concentrations were higher in dried MFT
(chloride 10–300 mmol L−1; sulfate 1–100 mmol L−1) than in CTS
(chloride 0.01–0.1 mmol L−1; sulfate 1.4–22 mmol L−1). For dried
MFT mean sodium concentration (20–300 mmol L−1) was higher
than for CTS (0.4–50 mmol L−1).
Sandy soil and CTS were air dried and sieved (b2mmfraction).MFT
was air dried, and ground to powder with a crusher, allowing for thorough
mixing with CTS. MFT was applied as a mixture with CTS (1:1)
(hereafter tailings mix), to reduce its toxic and hydrophobic properties.
Thus therewere three substrates: pure CTS, tailingsmix (CTS plus MFT)
and pure sandy soil. All substrates were sterilized by gamma radiation
(50 to 90 kGy for 24 h, Synergy Health GmbH, Radeberg, Germany) to
eliminate indigenous soil microorganisms.
2.2. Microbial materials
Three AMF species were used in equal proportions as fungal inoculum
for the two plant species. Funneliformis mosseae (former Glomus
mosseae), Rhizophagus intraradices (former Glomus intraradices) and
Claroideoglomus etunicatum (former Glomus etunicatum). Inocula were
purchased as granules including spores and fungal hyphae (200 propagules
per gram granules; pathogen and bacteria free) from Aurea
Systems GmbH, Neumarkt, Germany.
The bacterial suspensionwas composed of 18 bacterial strainswhich
were potential hydrocarbon degraders or typical soil and rhizosphere
bacteria (Table 1). All strains were isolated from oil sands derived byproducts
such as processed mature fine tailings (dried mature fine tailings)
and from bulk soil of tailings sands from a reclamation site in the
Athabasca oil sands mining site, Canada (Noah et al., 2014). Bacteria
were grown in tryptone soy medium until late log phase. 

Katja Boldt-Burisch a,⁎, M. Anne Naeth b, Uwe Schneider a, Beate Schneider c, Reinhard F. Hüttl a

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