Advertisement

Endophytes as Pollutant-Degrading Agents: Current Trends and Perspectives

  • Rúbia Carvalho Gomes Corrêa
  • Daiane Iark
  • Andressa de Sousa Idelfonso
  • Thais Marques Uber
  • Adelar Bracht
  • Rosane Marina PeraltaEmail author
Reference work entry
Part of the Reference Series in Phytochemistry book series (RSP)

Abstract

Bioremediation is based on biological systems, bacteria, fungi, and plants. They are effective systems to treat a polluted site because they are able to modify the chemical structure of the contaminant into less hazardous end products. Investigations regarding the theme have immensely accelerated during the last years, what originated a great number of articles involving the terms “phytoremediation” and “bioremediation.” Initially the term phytoremediation was defined as being the use of plants for the degradation of polluting hazardous chemicals. However, the discovery that healthy plants could be containing endosymbiotic groups of microorganisms, often bacteria or fungi, led to the notion that these microorganisms could be, partly at least, responsible for the degradation of the pollutants. This review focuses on this proposed partnership in the bioremediation process, taking into account investigations conducted during the last 5 years.

Keywords

Bioremediation Endophytes Pollutant-degrading agents Phytoremediation Xenobiotics 

1 Introduction

Industrial processes, agricultural practices, and the use of chemicals in many areas of our daily lives result in the deliberate or accidental release of potentially toxic chemicals into the environment. Environmental chemicals of particular concern include petroleum hydrocarbons, halogenated solvents from industrial sources, polycyclic aromatic hydrocarbons, endocrine-disrupting agents, pharmaceutical and personal care products, explosives, agricultural chemicals, and heavy metals, among others [1, 2].

The impact of hazardous xenobiotic residues on the environment has led to the necessity of finding feasible technologies to remediate these sites. The conventional remediation methods use physical and chemical processes, such as incineration, adsorption on resins and UV irradiation [3]. These methods generally result in excellent contaminant removal. However, from an ecological viewpoint, they are not friendly because they produce unwanted by-products and hazardous residues, besides generating the danger of human exposure to contaminants. An innovative technology for complementing or substituting the conventional methods and which presents the same or an even improved efficiency is bioremediation. By definition, bioremediation is the use of biological processes to clean up polluted sites. Such biological methods have the potential of being less expensive and more eco-friendly than physical and chemical treatments [4, 5]. Bioremediation is based on biological systems, bacteria, fungi, and plants. They are effective systems to treat a polluted site because they are able to modify the chemical structure of the contaminant into less hazardous end products [6]. Investigations regarding the theme have immensely accelerated during the last 10 years, what originated a great number of articles involving the terms “phytoremediation” and “bioremediation,” 10.441 and 20.560, respectively (data obtained from Web of Science, May 2018). Originally the term phytoremediation was defined as being the use of plants for the degradation of polluting hazardous chemicals. However, the discovery that healthy plants could be containing endosymbiotic groups of microorganisms, often bacteria or fungi, led to the idea that these microorganisms could be, partly at least, responsible for the degradation of the pollutants. The present review focuses on this proposed partnership in the bioremediation process, considering mainly experimental results published in the last 5 years.

2 Endophytes as Promising Pollutant-Degrading Agents

Endophytes are defined as fungi or bacteria which, for all or part of their life cycle, invade the tissues of living plants and cause unapparent and asymptomatic infections entirely within the plant tissues, but no symptoms of disease [7]. It is also important to note that plants can contain a mixture of colonizing endophytes, and not just a single species. In cases of both fungal endophyte- and bacterial endophyte-plant interactions, positive effects reported for plants involve overall biomass and growth enhancement, as well as enhanced biotic and abiotic stress tolerance [8, 9, 10]. In recent years, many studies demonstrated that endophytes are helpful in the remediation of contaminated soil, improve plant growth, and generate higher levels of soil activity. Since 2007, there has been a 15-fold increase in the number of publications addressing the theme of phytoremediation assisted by endophytic microorganisms (Fig. 1). Phytoremediation by plant–endophyte partnership is, consequently, an emerging, efficient, and eco-friendly technology, which consists in the use of plants and their associated microbes to clean up pollutants from the soil, water, and air [11, 12].
Fig. 1

Number of research articles and reviews published in the period from 2007 to 2017 regarding both “endophytic” and “phytoremediation” issues (obtained from Web of Science, May 2018; keywords restricted to the topics: endophytic and phytoremediation)

Being an area of active current investigation, novel efficient pollutant hyperaccumulators are being constantly prospected for utilization in phytoremediation and phytomining. In addition, molecular tools are being applied to improve knowledge on the mechanisms of xenobiotic uptake, translocation, sequestration, and tolerance in plants [3]. In the past years, several investigations have documented the endophyte-assisted phytoremediation as a promising approach for in situ bioremediation of contaminated areas [11, 12, 13, 14, 15].

Endophytes improve bioremediation processes through diverse ways, as they minimize heavy metal stress to plants [9], degrade toxicant components and metabolites released by plants [6], eliminate greenhouse gases from air [15], and finally control plague development in plant hosts [16]. They make the adaptation of plants to contaminated areas viable by providing the host with the required degradation pathways and metabolic abilities for diminishing phytotoxicity while enhancing plant growth through nitrogen fixation, mineral solubilization, and generation of phytohormones and siderophores, utilizing 1-aminocyclopropane-1-carboxylic acid as N source and via nutrient transformation [2, 6]. Moreover, this biodegradation strategy can also have a role in reducing the residual concentration of potentially toxic compounds in food crops, thus contributing to food safety [4].

In cases where genetic engineering of a xenobiotic degradation pathway is requested, bacteria are easier to manipulate than plants. Moreover, quantitative gene expression of pollutant catabolic genes within the endophytic populations could be a convenient tracking tool for evaluating the remediation efficiency. The special niche of the interior plant environment allows the pollutant degrader microorganism to achieve larger population sizes owing to the reduced competition [17]. Finally, an additional benefit of using endophytic pollutant degraders is that any intoxicant xenobiotics absorbed by the plant may be broken down in planta, thus minimizing phytotoxic effects and suppressing any harm to the fauna surrounding the contaminated areas [17].

Many endophytic microorganisms display a natural competence for xenobiotic degradation or may operate as vectors to insert degradative traits [4]. Such capacity to resist to heavy metals and antimicrobial agents and disintegrate organic compounds likely stems from their exposure to distinct compounds in the plant/soil niche. In the past 5 years, endophytes’ natural ability to degrade xenobiotics was approached in some review papers. The majority of the reviews in this field prioritized prospection and the advances in the exploitation of endophytic bacteria to assist the phytoremediation of pollutants [4, 5, 6, 11, 12, 13, 14], whereas only few papers focused on the use of fungal endophytes for this purpose [10, 18, 19].

2.1 Endophytic Bacteria

Plant–endophytic bacteria partnerships have been prospected for boosting the phytoremediation capacity of plants growing in areas infected with diversified organic compounds. There are several reports on the successful phytoremediation of polycyclic aromatic hydrocarbon (PAHs)-polluted sites using the plant-endophytic bacteria approach [20, 21, 22]. For instance, it has been found that the inoculation of willow and grass clones with the endophytic bacterial strain Pseudomonas putida PD1 caused a substantial reduction in the phytotoxicity of phenanthrene while promoting root and shoot growth [20]. Furthermore, it improved the removal (up to 40%) of phenanthrene from soil by host plants when compared to the uninoculated controls. Additionally, endophytic bacteria have been effectively applied to assist the phytoremediation of plants/lands contaminated with other organic compounds, such as pesticides like chlorpyrifos [2, 16], petroleum hydrocarbons [12, 23, 24], and toluene [25] (Table 1).
Table 1

Past 5-year experimental reports regarding bacterial endophyte-assisted phytoremediation of polluted sites and/or industrial effluents

Endophytic bacteria

Degraded pollutant main findings

Plant host

Bacillus thuringiensis GDB-1

Arsenic (As), cadmium (Cd), copper (Cu), zinc (Zn), and nickel (Ni): GDB-1 enhanced the growth of A. firma seedlings by virtue of 1-aminocyclopropane-1-carboxylic acid deaminase activity, indole acetic acid, and siderophore production, besides phosphorus solubilization. Inoculating A. firma with a GDB-1 strain alleviated the metabolic perturbations and stress induced by high concentrations of heavy metals and enhanced biomass as well as metal accumulation by the plant [26]

Alnus firma Siebold & Zucc.

Rahnella sp. JN6

Cd, Pb, and Zn: JN6-inoculated plants presented significantly higher dry weights, enhanced concentrations, and increased uptake of Cd, Pb, and Zn in both above-ground and root tissues when compared to non-inoculated controls and when growing in soils amended with Cd (25 mg kg−1), Pb (200 mg kg−1), or Zn (200 mg kg−1) [27]

Brassica napus L.

Achromobacter xylosoxidans F3B

Toluene, an aromatic hydrocarbon that can cause severe neurological harm: The strain F3B enhanced the degradation of toluene in vetiver, what resulted in a decrease in the phytotoxicity of the compound and a 30% reduction of its evapotranspiration through the leaves. Importantly, Achromobacter xylosoxidans F3B was able to maintain a stable population in plant roots without greatly interfering with the diversity of native endophytes [25]

Chrysopogon zizanioides (L.) Roberty

Burkholderia sp. SaZR4, Burkholderia sp. SaMR10, Sphingomonas sp. SaMR12, Variovorax sp. SaNR1

Zn and Cd: SaMR10 exhibited the smallest total population in plant’s tissues and minor impact on S. alfredii growth and phytoextraction, whereas SaZR4 significantly upgraded Zn-extraction, however, not Cd-extraction. SaMR12 and SaNR1 significantly enhanced plant growth on substrates supplemented with Zn or Cd as well as the phytoextraction of Zn and Cd [28]

Sedum alfredii Hance

Pseudomonas sp. Lk9

Cd, Zn, and Cu: Inoculation of S. nigrum with Lk9 enhanced the phytoextraction of Cd, Zn, and Cu. It improved soil’s Fe, P mineral nutrition supplies, as well as soil Cd, Zn, and Cu bioavailability. Moreover, Lk9 tolerated high levels of metal pollution and produced biosurfactants, siderophores, and organic acids [29]

Solanum nigrum L.

Pseudomonas monteilii PsF84, Pseudomonas plecoglossicida PsF610

Hexavalent chromium [Cr(VI)], a toxic and mobile form of the metal: Considering the biomass and Cr(VI) uptake in P. graveolens tissues, the total metal uptake in plant tissues per pot was notably superior in endophyte-inoculated plants when compared to the non-inoculated ones [30]

Pelargonium graveolens L’Hér. (rose scented geranium)

Pseudomonas putida PD1

Phenanthrene, a polycyclic aromatic hydrocarbon (PAH) compound: The inoculation of two different willow clones and a grass with PD1 allowed a substantial reduction in the phytotoxicity of phenanthrene while promoting root and shoot growth. Furthermore, it improved the removal (25–40%) of phenanthrene from soil by the tested host plants, when compared to the uninoculated controls [20]

Salix purpurea L. and Salix discolor Muhl.; Lolium spp.

Microbacterium arborescens TYSI04 and Bacillus pumilus PIRI30

Textile effluents: The combined plant-bacteria approach promoted, within 72 h, significant reductions in chemical oxygen demand (79%), biological oxygen demand (77%), total dissolved solids (59%), and total suspended solids (27%) of four assessed textile effluents [31]

Typha domingensis Pers.

Pseudomonas sp. Ph6-gfp

Phenanthrene, a polycyclic aromatic hydrocarbon (PAH) compound: Strain Ph6-gfp inoculation diminished the risk of PAH contamination in plant’s shoots and roots, thus showing its capacity of resisting to phenanthrene in planta [21]

Lolium multiflorum Lam.

Pseudomonas sp. J4AJ

Diesel, a toxic mixture of paraffin, cyclic alkenes, and aromatic compounds: The soils planted with S. triqueter and inoculated with J4AJ exhibited the highest diesel removal ratio (more than 54%) after 60-day experiment. However, the removal ratio of J4AJ-treated soils was near to 39%. The plant height and stem biomass in the J4AJ-inoculated soils significantly increased. The synergistic effect of S. triqueter and J4AJ also improved the activities of catalase and dehydrogenase in the soil [23]

Scirpus triqueter L.

Pseudomonas koreensis AGB-1

As, Cd, Cu, Pb, and Zn: M. sinensis inoculation with AGB-1 incremented heavy metal availability in the rhizosphere, lessened plant’s stress to metals and therefore its growth, and finally boosted metal uptake. AGB-1-inoculated plants phytostabilized and phytoremediated mine site soil [32]

Miscanthus sinensis Andersson

Azospirillum spp. and Pseudomonas stutzeri

Anthracene, phenanthrene, and pyrene, all PAHs, and diesel: The authors reported a statistically important increase in the physical properties of soils polluted with PAHs and diesel fuel compared with the control and a significant decrease in the content of PAHs and heavy metals in soils inoculated with Azospirillum spp. and P. stutzeri after D. glomerata growth [22]

Dactylis glomerata L.

Bacillus pumilus E2S2, Bacillus sp. E1S2, Bacillus sp. E4S1, Achromobacter sp. E4L5, and Stenotrophomonas sp. E1L

Cd and Zn: The tested endophytic bacterial strains increased the water extractable Cd and Zn concentrations in soil. E2S2 bettered the performance and metal uptake of S. plumbizincicola, likely through the generation of growth-promoting metabolites and production of metal-mobilizing enzymes. The isolated endophytes enhanced the phytoextraction capacity of S. plumbizincicola [33]

Sedum plumbizincicola X.H. Guo et S.B. Zhou ex L.H. Wu

41 bacteria belonging to Bacillus, Microbacterium, and Halomonas genera

Textile effluent: Among the strains demonstrating maximum efficiency of textile effluent degradation, eight of them displayed plant growth-promoting characteristics, namely, production of indole-3-acetic acid and siderophore, presence of 1-amino-cyclopropane-1-carboxylic acid deaminase, and solubilization of inorganic phosphorous. T. domingensis not only exhibited superior growth in textile effluent but also hosted the utmost number of endophytic bacteria [34]

Typha domingensis Pers., Pistia stratiotes L., Eichhornia crassipes (Mart.) Solms

Sphingomonas sp. U33, Bacillus sp. R12, Ochrobactrum sp. R24

Emerging organic contaminants (EOCs) and metals (Zn, Ni, Cd): The advantageous outcome of bioaugmentation with selected endophytes was more expressive in the exposure to high contamination, where most of the inoculated plants degraded the uppermost percentages of xenobiotics in shorter periods when compared to the control plants [35]

Juncus acutus L.

Bacillus pumilus DSKP8; 43 As-resistant bacteria, from Proteobacteria and Actinobacteria phyla

As: Strain DSKP8 can enhance growth as well as the uptake of arsenic by plants and may be exploited for cleaning up arsenic contaminated sites together with hyperaccumulators such as P. vittata. In the presence of 10 mM arsenate, six endophytic bacterial strains had greater growth than the control, thus indicating a stimulated development [36, 37]

Pteris vittata L.

Sphingomonas sp. HJY

Chlorpyrifos, toxic synthetic pesticides: Marked with the gfp gene, strain HJY successfully colonized Allium tuberosum diverse tissues and improved the degradation of chlorpyrifos inside the plants. Later, strain HJY displayed potential for reducing chlorpyrifos residues in A. tuberosum [2, 16]

Allium tuberosum Rottler ex Spreng.

Rhodococcus erythropolis, Ensifer adhaerens, Variovorax paradoxus, Phyllobacterium myrsinacearum

As: Betula celtiberica inoculation with R. erythropolis and E. adhaerens promoted an in vitro increase in total nonprotein thiols content in roots, indicating a detoxification mechanism via phytochelatin complexation. Furthermore, E. adhaerens inoculation boosted plant growth, while inoculation with the consortium comprising V. paradoxus and P. myrsinacearum improved As accumulation in the host roots [38]

Betula celtiberica (Rothm. & Vasc.)

26 hydrocarbon-degrading strains from Rhizobium, Pseudomonas, Stenotrophomonas, and Rhodococcus genera

Petroleum hydrocarbons: All assessed strains displayed at least one plant growth-promoting trait and possessed genes encoding for the hydrocarbon degradation enzymes. The endophytes were capable to develop in the presence of crude oil, diesel oil (more than 90% of the bacteria), and n-hexadecane (20% of the strains) [24]

Lotus corniculatus L., Oenothera biennis L.

Pantoea stewartii ASI11, Microbacterium arborescens HU33, Enterobacter sp. HU38

Tannery effluent: Constructed wetlands, vegetated only with L. fusca, indeed remediated tannery effluent; however, augmentation with endophytic bacteria not only efficiently stimulated the plant growth but also enhanced the removal of both organic and inorganic pollutants from the tannery effluent, also reducing its toxicity [39]

Leptochloa fusca (L.) Kunth

Constructed wetlands (CW) are sustainable eco-friendly systems employed for treating diverse kinds of effluents (varying from domestic to industrial toxicant wastewaters) which exploit the capacity of plants, together with their associated microorganisms, in clearing up organic compounds and metals from the water. In parallel with the biological processes, complex physical and chemical processes occur in the system, boosting the elimination of contaminants [40]. Shehzadi et al. [31] investigated, in a vertical flow CW reactor, the effects of the inoculation of two textile endophytic strains, Microbacterium arborescens TYSI04 and Bacillus pumilus PIRI30, on the detoxification efficiency of the wetland plant Typha domingensis. According to the authors, the combined plant-bacteria approach promoted, within a period of 72 h, significant reductions in chemical oxygen demand (79%), biological oxygen demand (77%), total dissolved solids (59%), and total suspended solids (27%) of four assessed textile effluents. Moreover, T. domingensis growth was improved, and there was a reduction in the effluent’s mutagenicity. Syranidou et al. [35] studied, for the first time, the potential of endophytic bacteria in upgrading the efficiency of wetland helophyte Juncus acutus. They reported positive results with respect to its capacity of removing emerging organic contaminants together with metals in simulated wetland systems. Very recently, Ashraf et al. [39] assessed the potential of a consortium of endophytic bacteria for bioaugmentation (application of indigenous or allochthonous wild type or genetically modified microorganisms to polluted hazardous waste site in order to accelerate the removal of undesired compounds) in a vertical flow CW vegetated with Leptochloa fusca. CW vegetated with only L. fusca indeed remediated the tannery effluent. However, bioaugmentation with Pantoea stewartii ASI11, Microbacterium arborescens HU33, and Enterobacter sp. HU38 not only stimulated the plant growth but also enhanced the removal of both organic and inorganic pollutants from the effluent, thus reducing its toxicity. Authors concluded that plant-endophyte partnerships make constructed wetlands a more powerful technique for the removal of organic and inorganic xenobiotics from wastewater than the plants employed alone.

Heavy metals cause serious toxic outcomes in plants, animals, and human health; thence, their remediation is mandatory. In the midst of the miscellaneous approaches that were employed, phytoremediation stands out as a modern, effective, and extremely safe tool for this end [41]. According to Ma et al. [11], endophytic bacteria ameliorate plant development in metal-contaminated soils via two means: (1) directly, through the generation of plant growth favorable substances, comprising solubilization/transformation of mineral nutrients and production of phytohormones, siderophores, and specific enzymes and (2) indirectly, by the biocontrol of pathogens or by inducing in plant hosts a systemic resistance against pathogens. In addition, they can shift the metal accumulation ability in plants by excreting metal-immobilizing extracellular polymeric substances and/or metal-mobilizing organic acids and biosurfactants.

Babu et al. [32] investigated the potential of Pseudomonas koreensis AGB-1 in association with Miscanthus sinensis to bioremediate mining site soil contaminated with arsenic, cadmium, copper, lead, and zinc. According to the authors, the inoculation of M. sinensis with the AGB-1 strain incremented heavy metal availability in the rhizosphere, lessened plant’s stress to metals and therefore its development, and finally boosted metal uptake. More recently, Xu et al. [37] assessed the potential of 43 arsenic-resistant endophytic bacteria isolated from Pteris vittata, an arsenic hyperaccumulator plant. In the presence of 10 mM arsenate, six bacterium endophytes had greater growth than the control, thus indicating arsenic-stimulated development. Results demonstrated that arsenic-resistant endophytes might improve P. vittata growth, thus enhancing its phytoextraction activity in arsenic-contaminated sites. Last but not least, endophytic bacteria can be engineered to improve heavy metal resistance/degradation systems and to remove organic toxic compounds present in soil [4, 11].

In the past 10 years, autofluorescent protein (AFP) techniques have figured as fundamental tools for investigating processes such as endophytes–plant interactions and biofilm formation [17]. These methodologies have been applied to detect and count microorganisms in situ on the plant exterior and in planta. One of the AFP’s strategies, the green fluorescent protein (GFP) gene marker, has been largely applied to visualize and monitor the colonization patterns of bacterial strains within inoculated plants, allowing a visual phenotype for investigating microorganisms’ population dynamics within vegetable tissues [20, 21]. Sun et al. [21] isolated the endophytic bacterium Pseudomonas sp. Ph6 from clover (Trifolium pratense) grown in PAH-contaminated soil and tagged it with the green fluorescent protein (GFP) gene in order to investigate its colonization and performance on PAH uptake by ryegrass. The authors could directly visualize, for the first time, its colonization and distribution in plant roots, stems, and leaves of ryegrass.

Despite the aforementioned evidence, the relevance of plant–endophyte synergisms for the removal of xenobiotics is presently undervalued. As many endophytic bacteria present pollutant-degrading, plant growth-promoting potentialities, and commonly both attributes, unravelling the mechanisms involved in these activities is a mandatory step to improve the phytoremediation of organic pollutants present in soil and water and expand its use in practice [4].

Babu et al. [26] found that the endophytic Bacillus thuringiensis GDB-1 had removal capacities of 77% for lead, 64% for zinc, 34% for arsenic, 9% for cadmium, 8% for copper, and 8% for nickel, throughout the growth cycle in a medium composed of heavy metal-amended mine tailing extract. Govarthanan et al. [43] when investigating the in vitro potential of the bacterium strain Paenibacillus sp. RM isolated from the roots of Tridax procumbens for the bioremediation of metals found that it was significantly resistant to copper, zinc, lead, and arsenic. Moreover, in batch experiments, the endophytic bacteria removed substantial amounts of copper (59%) and zinc (51%).

Shi et al. [42] identified and characterized an acid-stable bacterial laccase (Lac4) produced by the endophyte Pantoea ananatis Sd-1 cultured in rice straw. Lac4, which also presented interesting lignin degradation potential, was able to decolorize various synthetic dyes. It displayed a superior decolorization efficiency with Aniline Blue (47%) and Congo red (89%) when compared to that with RBBR (35%) after 4 h in the presence of a mediator. With Congo red, the decolorization reached 60% after 2 h, in the absence of a mediator.

Recently, Feng et al. [16] assessed the chlorpyrifos-degrading potential of the strain Sphingomonas sp. HJY isolated from Chinese chives. Nearly 96% of 20 mg L−1 chlorpyrifos was removed by the endophyte at the end of a 15-day liquid culture experiment using a minimum salts medium. Authors determined the optimal conditions for chlorpyrifos removal and proposed, for the first time, a metabolic pathway for the degradation of chlorpyrifos by an endophytic bacterium of the genus Sphingomonas (Fig. 2).
Fig. 2

Possible metabolic pathways for chlorpyrifos degradation by Sphingomonas sp. strain HJY, as proposed by Feng et al. [16]. HPLC coupled to time-of-flight mass spectrometry analysis indicated that O,O-diethyl O-3,5,6-trichloropyridinol was the major degradation product of chlorpyrifos

Other examples of recent investigations addressing the potential of endophytic bacteria alone as xenobiotic degraders are shown in Table 2.
Table 2

Past few years major experimental papers reporting the in vitro potential of endophytic bacteria as pollutant-degrading agents

Endophytic bacteria

Degraded pollutant main findings

Plant host

Bacillus thuringiensis GDB-1

As, Cu, Pb, Ni, and Zn: GDB-1’s removal capacity was about 77% for Pb, 64% for Zn, 34% for As, 9% for Cd, 8% for Cu, and 8% for Ni throughout the growth cycle in medium composed of heavy metal-amended mine tailing extract [26]

Alnus firma Siebold & Zucc.

Pseudomonas koreensis AGB-1

As, Cd, Cu, Pb, and Zn: AGB-1 inoculation enhanced heavy metal(loid) solubilization in vitro. The isolated endophyte presents arsB, ACR3(1), aoxB, and bmtA marker genes for heavy metal resistance [32]

Miscanthus sinensis Andersson

Rahnella sp. JN6

Cd, Pb, and Zn: Strain JN6 displayed notable Cd, Pb, and Zn tolerance and competently solubilized CdCO3, PbCO3, and Zn3(PO4)2 in culture solution [27]

Polygonum pubescens Blume

Paenibacillus sp. RM

Cu, Zn, Pb, and As: Strain RM displayed a significant resistance to all tested heavy metals. In batch experiments RM performed high removal of Cu (59%) followed by Zn (51%) [43]

Tridax procumbens (L.) L.

8 isolates from Bacillus, Enterobacter, Stenotrophomonas, and Rhizobium genera

As: All endophytic isolates displayed tolerance to arsenic up to 1000 mg L−1, among which five isolates were indole acetic acid positive (highest production up to 60 mg/L). Presence of aox gene was confirmed in two strains and arsB gene in six isolates. The isolated strain named E4 was a good indole acetic acid producer as well as arsenic-tolerant [45]

Pteris vittata L.

Pseudomonas sp. Ph6-gfp

Phenanthrene, PAH compound: Ph6-gfp consumed more than 80% of phenanthrene in a culture solution (50 mg/L) within 15 days, evidencing its capacity to resist against phenanthrene in vitro [21]

Lolium multiflorum Lam.

Pseudomonas sp. J4AJ and Bacillus subtilis U-3

Diesel: J4AJ significantly degraded the n-alkane component of diesel, especially the short-chain hydrocarbons. Addition of the surfactant sodium lauroyl sarcosine to the system effectively improved the removal ratios of such compounds. The biosurfactant produced by the U-3 strain could also improve the removal ratios of most diesel’s n-alkanes [44]

Scirpus triqueter

Pantoea ananatis Sd-1

Congo red, Remazol Brilliant Blue R (RBBR), and Aniline Blue: A novel microbial laccase (Lac4) produced by Sd-1 displayed superior decolorization efficiency for Aniline Blue (47%) and Congo red (89%) than for RBBR (35%) after 4 h in the presence of a mediator. For Congo red, the decolorization reached 60% after 2 h in the absence of a mediator [42]

Oryza sp.

Stenotrophomonas sp. and Pseudomonas sp.

Mixed polycyclic aromatic hydrocarbons (PAHs): Both Stenotrophomonas sp. and Pseudomonas sp. were able to utilize PHAs as their exclusive sources of carbon and energy. In biodegradation studies, Stenotrophomonas sp. was able to consume 98% naphthalene, 83% fluoranthene, 87% phenanthrene, 14% pyrene, and 2% benzo(α)pyrene, while Pseudomonas sp. removed 95% naphthalene, 88% fluoranthene, 90% phenanthrene, and 7% pyrene, both after 7 days of inoculation [46]

Conyza canadensis L. Cronquist and Trifolium pretense L.

Sphingomonas sp. HJY

Chlorpyrifos, toxic synthetic pesticides: Authors investigated the degradation gene and proposed a metabolic pathway for the degradation of chlorpyrifos by HJY (Fig. 2), which was able to metabolize 96% of 20 mg L−1 chlorpyrifos during 15 days in liquid minimal salts medium [16]

Allium tuberosum Rottler ex Spreng.

2.2 Endophytic Fungi

In comparison to bacteria, most fungi display a filamentous growth trend, which allows to follow both explorative and exploitative growth strategies and to form linear organs of aggregated hyphae to safeguard fungal translocation. This capacity of translocating nutrients through the mycelia network is a relevant feature in colonizing heterogeneous environments [10]. In addition, the low specificity of their catabolic enzymes and their independence from utilizing xenobiotic compounds as growth substrates makes them strong candidates for bioremediation agents [1].

Endophytic fungi possess the biochemical and ecological capacity to degrade or solubilize organic, mineral, and metal pollutants, either by chemical modification (directly, by enzymatic action) or by influencing chemical bioavailability. The latter is accomplished, for example, through the excretion of metabolites and varied mechanisms, including acidolysis, complexolysis, redoxolysis, and metal accumulation in biomass [1, 19].

Although knowledge on the role of endophytic fungi in phytoremediation is limited, some recent papers have addressed their potential use in bioremediation processes (Table 3).
Table 3

Past 5-year major papers reporting the in vitro potential of endophytic fungi as pollutant-degrading agents

Endophytic fungi

Degraded pollutant main findings

Plant host

Phomopsis liquidambari B3

Indole, a typical N-heterocyclic compound: The addition of B3 to soil significantly promoted mineral N release by changing the distribution of soil organic nitrogen. Authors investigated its indole biodegradation potential at 100 mg L−1. The attendance of plant litter significantly incremented and speeded up fungal degradation activity. HPLC–MS and NMR analysis indicated the metabolic pathway: indole was first oxidized to oxindole and isatin and subsequently broke down the C–N position in the pyridine ring [47, 48]

Atractylodes lancea (Thunb.) DC.

Phomopsis liquidambari B3

Ferulic acid, a high-priority environmental pollutant: B3 was capable of using ferulic acid as its unique carbon source, efficaciously degrading the compound in mineral salt medium and soil. Authors proposed a degradation pathway: ferulic acid was firstly decarboxylated to 4-vinyl guaiacol and next oxidized to vanillin and vanillic acid, followed by demethylation to protocatechuic acid, which was further broken down through the β-ketoadipate pathway. Fungal laccase had a key role in the biodegradation process [49]

Bischofia polycarpa (H.Lév.) Airy Shaw

Phomopsis liquidambari B3

Cinnamic acid, a phenolic allelochemical: Strain B3 was able to effectively decompose cinnamic acid in mineral salt medium and soil, and the proposed metabolic pathway for the allelochemical degradation is shown in Fig. 3. The generation of laccase significantly enhanced the biodegradation process [50]

Bischofia polycarpa (H.Lév.) Airy Shaw

Cunninghamella echinulata, Pestalotiopsis sp., Hypoxylon anthochroum, Paecilomyces lilacinus, Aspergillus sp., and Lasiodiplodia theobromae

Gamma-irradiated low-density polyethylene (common plastic polymer) and polypropylene (thermoplastic polymer): Reductions on intrinsic viscosity and average molecular weight of gamma-irradiated semicrystalline low-density polyethylene strips inoculated with Aspergillus sp. and Paecilomyces lilacinus (both from H. brunonis) and Lasiodiplodia theobromae (from P. flavida) showed fungal effectiveness in plastic transformation. This study suggests that higher doses of gamma rays could increase plastics’ sensitivity toward microorganisms instead of guaranteeing sterilization of the material [51]

Psychotria flavida Talbot and Humboldtia brunonis Wall.

Phomopsis liquidambari B3

Luteolin, a common phytoestrogen: The optimum concentration for luteolin metabolization by B3 was 200 mg L−1, and the proposed degradation pathway is shown in Fig. 4. Genes encoding protocatechuate 3,4-dioxygenase and hydroxyquinol1,2-di-oxygenase enzymes were successfully cloned. Reverse-transcription quantitative polymerase chain reaction assays revealed the important role of these genes in catalyzing the ring fission during the biodegradation process [52]

Bischofia polycarpa (H.Lév.) Airy Shaw

Penicillium sp. FT2G59 and P. columnaris FT2G7

Pb, Zn, and Cd (heavy metals): In in vitro tolerance assays, FT2G59 tolerated Pb, Zn, and Cd with the MIC of 30–50, >680, 20–30 mmol/l, respectively, while FT2G7 tolerated Cd with the MIC of 30–50 mmol/l. Therefore, these endophytic strains displayed potential for phytoremediation of metal-contaminated sites [53]

Dysphania ambrosioides (L.) Mosyakin & Clemants

Phomopsis liquidambari B3

Sinapic acid, one of the most representative methoxy phenolic pollutants: Both in flasks and in the soil, almost 99% of the added sinapic acid (at the optimum concentration for biodegradation of 200 mg L−1) was consumed within 48 h by strain B3. The complete sinapic acid metabolic pathway was tentatively proposed for the first time (Fig. 5) [54]

Bischofia polycarpa (H.Lév.) Airy Shaw

Neurospora intermedia DP8–1

Diuron, a phenylurea herbicide classified as a priority hazardous substance: In biodegradation studies in liquid media, DP8-1 degraded up to 99% diuron within 3 days under the optimal degrading conditions. Moreover, it was able to utilize other phenylurea herbicides, namely, fenuron, monuron, metobromuron, isoproturon, chlorbromuron, linuron, and chlortoluron, as substrate for its growth. The main diuron metabolization pathway by strain DP8-1 consisted in sequential N-dealkylations [55]

Saccharum sp. (sugarcane)

Penicillium oxalicum B4

Triclosan, a widely used antimicrobial and preservative agent: The triclosan metabolization degree by strain B4 reached more than 97% at 1 h in liquid medium. Yet in non-sterile synthetic wastewater, only 2 h were required for the complete removal process. Compared to other microbial degraders, B4 presented a higher efficiency in removing triclosan [56]

Artemisia annua L.

Tong et al. [55, 57] performed a study on native grass species infected by endophytic fungi in a copper tailings dam through progressive years of phytoremediation. Authors not only found that the endophytic infection frequency raised over the years but also highlighted that the infection rates of Bothriochloa ischaemum and Festuca rubra were positively related to the cadmium pollution levels. Moreover, endophytic fungi colonizing Imperata cylindrical and Elymus dahuricus became tolerant to lead. Structure and relative ampleness of the bacterial communities had small fluctuations over the period; however, there was a marked variation in soil fungi species.

Chen et al. [47] demonstrated that the endophytic fungus Phomopsis liquidambari B3 was capable to promote in vitro the litter release of NH4+–N from plant litter to soil, thus enhancing soil inorganic N contents. This increment in NH4+–N, on its turn, boosted the soil ammonia-oxidizing bacteria community and enhanced nitrification, leading to an elevation in soil NO3−–N. Posteriorly, the same group investigated the biodegradation of N-heterocyclic indole (at 100 mg L−1) by strain B3 and reported a degradation ratio of almost 42% within 120 h. According to the authors, plant litter supplementation significantly incremented and speeded up the fungal degradation activity. Results obtained in HPLC–MS and nuclear magnetic resonance analyses provided the basis for suggesting a metabolic pathway for indole degradation by strain B3. Two non-specific oxidases induced by plant liter, namely, laccase and LiP, were key enzymes acting in the production of oxindole and transformation of isatin [48].

Xie and Dai [50] investigated the biodegradation of the model allelochemical cinnamic acid by P. liquidambari B3, with promising results. As shown in Fig. 3, cinnamic acid was initially transformed into styrene, which was further broken down sequentially into benzaldehyde, benzoic acid, 4-hydroxybenzoic acid, and protocatechuic acid, involving phenolic acid decarboxylase, laccase, hydroxylase, and protocatechuate 3,4-dioxygenase.
Fig. 3

Cinnamic acid biodegradation pathway by Phomopsis liquidambari, as proposed by Xie and Dai [50]. (1) Cinnamic acid decarboxylation; (2) styrene oxidation; (3) benzaldehyde oxidation; (4) benzoic acid hydroxylation; (5) hydroxybenzoic acid hydroxylation; (6) protocatechuic acid ring fission; and (7) entry into the TCA cycle

Wang et al. [52] also studied the remediation properties of P. liquidambari B3, this time its potential of degrading the phytoestrogen luteolin. The authors found that the optimum concentration for luteolin metabolization by strain B3 was 200 mg L−1. Further, they suggested that the compound was metabolized via caffeic acid and phloroglucinol into protocatechuic acid and hydroxyquinol, which were subsequently disjointed by dioxygenases (Fig. 4). Later, Xie et al. [54] assessed the potential of P. liquidambari B3 for transformation and biodegradation of the recalcitrant pollutant sinapic acid, a typical methoxy phenolic pollutant found in industrial wastewaters.
Fig. 4

The likely degradation pathway of luteolin by Phomopsis liquidambari, as proposed by Wang et al. [52]. Maleylacetate and β-carboxy-cis,cis-muconic acid are proposed intermediates and have not been isolated

Besides reporting an in vitro degradation rate of almost 99% within 48 h by the strain B3, authors tentatively proposed the complete sinapic acid degradation pathway (Fig. 5). The degrading enzyme activities, along with their gene transcription levels, notably varied throughout the degradation course and displayed a “cascade induction” response with the dynamics of substrate and metabolite concentrations.
Fig. 5

The biodegradation pathway of sinapic acid in Phomopsis liquidambari, according to Xie et al. [54]. (1) Sinapic acid decarboxylation; (2) 2,6-dimethoxy-4-vinylphenol oxidation; (3) 4-hydroxy-3,5-dimethoxybenzaldehyde oxidation; (4) syringic acid demethylation; (5) gallic acid ring fission; (6) citric acid goes into the citric acid cycle

3 Concluding Remarks and Future Prospects

The past 5 years investigations on the role of endophytes in the bioremediation of contaminated soils and waters reveal highly positive and promising prospects for future investigations. Most papers published over the period of the last 5 years addressed prospection and use of endophytic bacterial strains for enhancing phytoremediation. The potentiality of endophytic fungi, in contrast, in spite of the proposition of several metabolization mechanisms, has been uncovered for only a limited number of species. This is a fact duly taken into account in the series of future directions that we are proposing and that are also summarized in Fig. 6.
Fig. 6

Perspective of new studies of endophytes in bioremediation

  1. 1.

    Referring to the study of bacterial endophytes in bioremediation, further investigations should prioritize the assessment of the remediation potential of the bacteria alone (away from the plant environment). Moreover, the identification of the genes involved in their degradation abilities and the elucidation of the degradation pathways are needed.

     
  2. 2.

    Notably, the capacity of endophytic fungi as degraders of xenobiotics is still underexploited, and the discovery of new species, together with the detection of genes involved in such abilities seems to be of general interest.

     
  3. 3.

    Further investigations should consider to investigate the interaction and possible synergistic action of fungi and endophytic bacteria in phytoremediation.

     

Lastly, despite the past two decade’s significant advances, our knowledge regarding the potential of endophytes as pollutant-degrading agents is still incomplete. Hopefully in the future, the full potential of these microorganisms can be exploited for environmental and agricultural purposes.

Notes

Acknowledgments

The authors thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Proc. 404898/2016-5) for funding this study. R.C.G. Corrêa thanks CNPq for financing her postdoctoral research at State University of Maringá (Process number 167378/2017-1). R.M. Peralta (Project number 307944/2015-8) and A. Bracht (Project number 304090/2016-6) are CNPq research grant recipients.

References

  1. 1.
    Harms H, Schlosser D, Wick LY (2011) Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol 9:177–192CrossRefGoogle Scholar
  2. 2.
    Feng F, Ge J, Li Y, Cheng J, Zhong J, Yu X (2017) Isolation, colonization, and chlorpyrifos degradation mediation of the endophytic bacterium Sphingomonas strain HJY in Chinese chives (Allium tuberosum). Agric Food Chem 65:1131–1138CrossRefGoogle Scholar
  3. 3.
    Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals – concepts and applications. Chemosphere 91:869–881CrossRefGoogle Scholar
  4. 4.
    Afzal M, Khan QM, Sessitsch A (2014) Endophytic bacteria: prospects and applications for the phytoremediation of organic pollutants. Chemosphere 117:232–242CrossRefGoogle Scholar
  5. 5.
    Zhu X, Ni X, Liu J, Gao Y (2014) Application of endophytic bacteria to reduce persistent organic pollutants contamination in plants. Clean (Weinh) 42:306–310Google Scholar
  6. 6.
    Yadav A, Yadav K (2017) Exploring the potential of endophytes in agriculture: a minireview. Adv Plants Agric Res 6:00221Google Scholar
  7. 7.
    Corrêa RCG, Rhoden SA, Mota TR, Azevedo JL et al (2014) Endophytic fungi: expanding the arsenal of industrial enzyme producers. J Ind Microbiol Biotechnol 41:1467–1478CrossRefGoogle Scholar
  8. 8.
    Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: plant–endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254CrossRefGoogle Scholar
  9. 9.
    Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194CrossRefGoogle Scholar
  10. 10.
    Deng Z, Cao L (2017) Fungal endophytes and their interactions with plants in phytoremediation: a review. Chemosphere 168:1100–1106CrossRefGoogle Scholar
  11. 11.
    Ma Y, Rajkumar M, Zhang C, Freitas H (2016) Beneficial role of bacterial endophytes in heavy metal phytoremediation. J Environ Manag 174:14–25CrossRefGoogle Scholar
  12. 12.
    Gkorezis P, Daghio M, Franzetti A, Van Hamme JD, Sille W, Vangronsveld J (2016) The interaction between plants and bacteria in the remediation of petroleum hydrocarbons: an environmental perspective. Front Microbiol 7:1836CrossRefGoogle Scholar
  13. 13.
    Li HY, Wei DQ, Shen M, Zhou ZP (2012) Endophytes and their role in phytoremediation. Fungal Divers 54:11–18CrossRefGoogle Scholar
  14. 14.
    Stępniewska Z, Kuźniar A (2013) Endophytic microorganisms – promising applications in bioremediation of greenhouse gases. Appl Microbiol Biotechnol 97:9589–9596CrossRefGoogle Scholar
  15. 15.
    Gonzalez F, Tkaczuk C, Dinu MM, Fiedler Ż, Vidal S, Zchori-Fein E, Messelink GJ (2016) New opportunities for the integration of microorganisms into biological pest control systems in greenhouse crops. J Pest Sci 89:295–311CrossRefGoogle Scholar
  16. 16.
    Feng F, Li Y, Ge J et al (2017) Degradation of chlorpyrifos by an endophytic bacterium of the Sphingomonas genus (strain HJY) isolated from Chinese chives (Allium tuberosum). J Environ Sci Health B 52:736–744CrossRefGoogle Scholar
  17. 17.
    Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9CrossRefGoogle Scholar
  18. 18.
    Sudha V, Govindaraj R, Baskar K, Al-Dhabi NA, Duraipandiyan V (2016) Biological properties of endophytic fungi. Braz Arch Biol Technol 59:e16150436CrossRefGoogle Scholar
  19. 19.
    Naik BS (2017) Fungal endophytes: nature’s tool for bioremediation of toxic pollutants. Curr Sci 113:537–539CrossRefGoogle Scholar
  20. 20.
    Khan Z, Roman D, Kintz T, delas Alas M, Yap R, Doty S (2014) Degradation, phytoprotection and phytoremediation of phenanthrene by endophyte Pseudomonas putida PD1. Environ Sci Technol Lett 48:12221–12228CrossRefGoogle Scholar
  21. 21.
    Sun K, Liu J, Gao Y, Jin L, Gu Y, Wang W (2014) Isolation, plant colonization potential, and phenanthrene degradation performance of the endophytic bacterium Pseudomonas sp. Ph6-gfp. Sci Rep 4:5462CrossRefGoogle Scholar
  22. 22.
    Gałązka A, Gałązka R (2015) Phytoremediation of polycyclic aromatic hydrocarbons in soils artificially polluted using plant-associated-endophytic bacteria and Dactylis glomerata as the bioremediation plant. Pol J Microbiol 64:239–250CrossRefGoogle Scholar
  23. 23.
    Zhang X, Chen L, Liu X, Wang C, Chen X, Xu G, Deng K (2014) Synergic degradation of diesel by Scirpus triqueter and its endophytic bacteria. Environ Sci Pollut Res Int 21:8198–8205CrossRefGoogle Scholar
  24. 24.
    Pawlik M, Cania B, Thijs S, Vangronsveld J, Piotrowska-Seget Z (2017) Hydrocarbon degradation potential and plant growth-promoting activity of culturable endophytic bacteria of Lotus corniculatus and Oenothera biennis from a long-term polluted site. Environ Sci Pollut Res Int 24:19640–19652CrossRefGoogle Scholar
  25. 25.
    Ho Y-N, Hsieh J-L, Huang C-C (2013) Construction of a plant–microbe phytoremediation system: combination of vetiver grass with a functional endophytic bacterium, Achromobacter xylosoxidans F3B, for aromatic pollutants removal. Bioresour Technol 145:43–47CrossRefGoogle Scholar
  26. 26.
    Babu AG, Kim JD, Oh BT (2013) Enhancement of heavy metal phytoremediation by Alnus firma with endophytic Bacillus thuringiensis GDB-1. J Hazard Mater 250:477–483CrossRefGoogle Scholar
  27. 27.
    He H, Ye Z, Yang D, Yan J et al (2013) Characterization of endophytic Rahnella sp. JN6 from Polygonum pubescens and its potential in promoting growth and Cd, Pb, Zn uptake by Brassica napus. Chemosphere 90:1960–1965CrossRefGoogle Scholar
  28. 28.
    Zhang X, Lin L, Zhu Z, Yang X, Wang Y, An Q (2013) Colonization and modulation of host growth and metal uptake by endophytic bacteria of Sedum alfredii. Int J Phytoremediation 15:51–64CrossRefGoogle Scholar
  29. 29.
    Chen L, Luo S, Li X, Wan Y, Chen J, Liu C (2014) Interaction of Cd-hyperaccumulator Solanum nigrum L. and functional endophyte Pseudomonas sp. Lk9 on soil heavy metals uptake. Soil Biol Biochem 68:300–308CrossRefGoogle Scholar
  30. 30.
    Dharni S, Srivastava AK, Samad A, Patra DD (2014) Impact of plant growth promoting Pseudomonas monteilii PsF84 and Pseudomonas plecoglossicida PsF610 on metal uptake and production of secondary metabolite (monoterpenes) by rose-scented geranium (Pelargonium graveolens cv. bourbon) grown on tannery sludge amended soil. Chemosphere 117:433–439CrossRefGoogle Scholar
  31. 31.
    Shehzadi M, Afzal M, Khan MU, Islam E, Mobin A, Anwar S, Khan QM (2014) Enhanced degradation of textile effluent in constructed wetland system using Typha domingensis and textile effluent-degrading endophytic bacteria. Water Res 58:152–159CrossRefGoogle Scholar
  32. 32.
    Babu AG, Shea PJ, Sudhakar D, Jung IB, Oh BT (2015) Potential use of Pseudomonas koreensis AGB-1 in association with Miscanthus sinensis to remediate heavy metal (loid)-contaminated mining site soil. J Environ Manag 151:160–166CrossRefGoogle Scholar
  33. 33.
    Ma Y, Oliveira RS, Nai F, Rajkumar M, Luo Y, Rocha I, Freitas H (2015) The hyperaccumulator Sedum plumbizincicola harbors metal-resistant endophytic bacteria that improve its phytoextraction capacity in multi-metal contaminated soil. J Environ Manag 156:62–69CrossRefGoogle Scholar
  34. 34.
    Shehzadi M, Fatima K, Imran A, Mirza MS, Khan QM, Afzal M (2016) Ecology of bacterial endophytes associated with wetland plants growing in textile effluent for pollutant-degradation and plant growth-promotion potentials. Plant Biosyst 150:1261–1270CrossRefGoogle Scholar
  35. 35.
    Syranidou E, Christofilopoulos S, Gkavrou G, Thijs S, Weyens N, Vangronsveld J, Kalogerakis N (2016) Exploitation of endophytic bacteria to enhance the phytoremediation potential of the wetland helophyte Juncus acutus. Front Microbiol 7:1016CrossRefGoogle Scholar
  36. 36.
    Srivastava S, Singh M, Paul AK (2016) Arsenic bioremediation and bioactive potential of endophytic bacterium Bacillus pumilus isolated from Pteris vittata L. Int J Adv Biotechnol Res 7:77–92Google Scholar
  37. 37.
    Xu JY, Han YH, Chen Y, Zhu LJ, Ma LQ (2016) Arsenic transformation and plant growth promotion characteristics of As-resistant endophytic bacteria from As-hyperaccumulator Pteris vittata. Chemosphere 144:1233–1240CrossRefGoogle Scholar
  38. 38.
    Mesa V, Navazas A, González-Gil R, González A et al (2017) Use of endophytic and rhizosphere bacteria to improve phytoremediation of arsenic-contaminated industrial soils by autochthonous Betula celtiberica. Appl Environ Microbiol 83:e03411–e03416CrossRefGoogle Scholar
  39. 39.
    Ashraf S, Afzal M, Naveed M, Shahid M, Ahmad Zahir Z (2018) Endophytic bacteria enhance remediation of tannery effluent in constructed wetlands vegetated with Leptochloa fusca. Int J Phytoremediation 20:121–128CrossRefGoogle Scholar
  40. 40.
    Wu H, Zhang J, Ngo HH, Guo W, Hu Z et al (2015) A review on the sustainability of constructed wetlands for wastewater treatment: design and operation. Bioresour Technol 175:594–601CrossRefGoogle Scholar
  41. 41.
    Ullah A, Heng S, Munis MFH, Fahad S, Yang X (2015) Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review. Environ Exp Bot 117:28–40CrossRefGoogle Scholar
  42. 42.
    Shi X, Liu Q, Ma J et al (2015) An acid-stable bacterial laccase identified from the endophyte Pantoea ananatis Sd-1 genome exhibiting lignin degradation and dye decolorization abilities. Biotechnol Lett 37:2279–2288CrossRefGoogle Scholar
  43. 43.
    Govarthanan M, Mythili R, Selvankumar T, Kamala-Kannan S, Rajasekar A, Chang YC (2016) Bioremediation of heavy metals using an endophytic bacterium Paenibacillus sp. RM isolated from the roots of Tridax procumbens. 3 Biotech 6:242CrossRefGoogle Scholar
  44. 44.
    Zhang X, Liu X, Wang Q, Chen X, Li H, Wei J, Xu G (2014) Diesel degradation potential of endophytic bacteria isolated from Scirpus triqueter. Int Biodeterior Biodegrad 87:99–105CrossRefGoogle Scholar
  45. 45.
    Tiwari S, Sarangi BK, Thul ST (2016) Identification of arsenic resistant endophytic bacteria from Pteris vittata roots and characterization for arsenic remediation application. J Environ Manag 180:359–365CrossRefGoogle Scholar
  46. 46.
    Zhu X, Ni X, Waigi MG, Liu J, Sun K, Gao Y (2016) Biodegradation of mixed PAHs by PAH-degrading endophytic bacteria. Int J Environ Res Public Health 13:805CrossRefGoogle Scholar
  47. 47.
    Chen Y, Ren CG, Yang B, Peng Y, Dai CC (2013) Priming effects of the endophytic fungus Phomopsis liquidambari on soil mineral N transformations. Microb Ecol 65:161–170CrossRefGoogle Scholar
  48. 48.
    Chen Y, Xie XG, Ren CG, Dai CC (2013) Degradation of N-heterocyclic indole by a novel endophytic fungus Phomopsis liquidambari. Bioresour Technol 129:568–574CrossRefGoogle Scholar
  49. 49.
    Xie XG, Dai CC (2015) Degradation of a model pollutant ferulic acid by the endophytic fungus Phomopsis liquidambari. Bioresour Technol 179:35–42CrossRefGoogle Scholar
  50. 50.
    Xie XG, Dai CC (2015) Biodegradation of a model allelochemical cinnamic acid by a novel endophytic fungus Phomopsis liquidambari. Int Biodeterior Biodegrad 104:498–507CrossRefGoogle Scholar
  51. 51.
    Sheik S, Chandrashekar KR, Swaroop K, Somashekarappa HM (2015) Biodegradation of gamma irradiated low density polyethylene and polypropylene by endophytic fungi. Int Biodeterior Biodegrad 105:21–29CrossRefGoogle Scholar
  52. 52.
    Wang HW, Zhang W, Su CL, Zhu H, Dai CC (2015) Biodegradation of the phytoestrogen luteolin by the endophytic fungus Phomopsis liquidambari. Biodegradation 26:197–210CrossRefGoogle Scholar
  53. 53.
    Li X, Li W, Chu L, White JF Jr, Xiong Z, Li H (2016) Diversity and heavy metal tolerance of endophytic fungi from Dysphania ambrosioides, a hyperaccumulator from Pb–Zn contaminated soils. Arthropod Plant Interact 11:186–192CrossRefGoogle Scholar
  54. 54.
    Xie XG, Huang CY, Fu WQ, Dai CC (2016) Potential of endophytic fungus Phomopsis liquidambari for transformation and degradation of recalcitrant pollutant sinapic acid. Fungal Biol 120:402–413CrossRefGoogle Scholar
  55. 55.
    Wang Y, Li H, Feng G, Du L, Zeng D (2017) Biodegradation of diuron by an endophytic fungus Neurospora intermedia DP8-1 isolated from sugarcane and its potential for remediating diuron-contaminated soils. PLoS One 12:e0182556CrossRefGoogle Scholar
  56. 56.
    Tian H, Ma YJ, Li WY, Wang JW (2018) Efficient degradation of triclosan by an endophytic fungus Penicillium oxalicum B4. Environ Sci Pollut Res Int 25:8963–8989CrossRefGoogle Scholar
  57. 57.
    Tong J, Miaowen C, Juhui J, Jinxian L, Baofeng C (2017) Endophytic fungi and soil microbial community characteristics over different years of phytoremediation in a copper tailings dam of Shanxi, China. Sci Total Environ 574:881–888CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Rúbia Carvalho Gomes Corrêa
    • 1
  • Daiane Iark
    • 1
  • Andressa de Sousa Idelfonso
    • 1
  • Thais Marques Uber
    • 1
  • Adelar Bracht
    • 1
    • 2
  • Rosane Marina Peralta
    • 1
    • 2
    Email author
  1. 1.State University of MaringaMaringáBrazil
  2. 2.Department of Biochemistry, Laboratory of Biochemistry of Microorganisms and Food ScienceState University of MaringaMaringáBrazil

Personalised recommendations