Research article
Biodegradation and utilization of crop residues contaminated with poisonous pyrrolizidine alkaloids

https://doi.org/10.1016/j.jenvman.2021.112629Get rights and content

Highlights

  • This study aims to evaluate possibilities to reduce the poisonous PA-content of the initial plant by composting or biogas.

  • The biodegradation of PAs from S. jacobaea and L. squarrosa was studied by model experiments and HPLC-ESI-MS/MS analysis.

  • The PA degradation was over 99% (3 months composting) and between 91 and 99% (4-weeks biomethanization).

  • The results are discussed in the light of re-utilzing PA-contaminated plant matter in a circular bioeconomy.

Abstract

Disposal of noxious plant residues is a challenge for farmers and land management dealing with contaminated biomasses. Recent studies confirm the potential threat of transferring toxic plant constituents like pyrrolizidine alkaloids (PAs) from plant residues to non-toxic succeeding agricultural crops via the soil.

We studied the degree of biochemical degradation of PAs in the two most important processes, composting and biomethanization. We used lab composting and biogas batches to investigate the potential of PA-degradation of two common PA-containing plants, Lappula squarrosa and Senecio jacobaea.

The experiments demonstrated a virtually complete loss of PAs in three months during the composting process and a rapid decomposition of PAs from 3112.6 μg/kg to less than 21.5 μg/kg in L. squarrosa and from 6350.2 μg/kg to less than 539.6 μg/kg in S. jacobaea during biomethanization. The information obtained is a first guide on how to re-utilize PA-contaminated plant matter in a circular bioeconomy.

Introduction

The promotion of a circular bioeconomy is considered necessary by many countries in order to solve the urgent problems of efficient and sustainable use of resources in the face of dwindling raw materials and increasing environmental impacts of a fossil-based, linear economy (Hetemäki et al., 2017). The agri-food sector, as a major pillar of the bioeconomy, is inherently linked to agricultural land use and offers countless opportunities to improve its circularity by reusing resources, valorizing by-products, and a cascading use of biomass (Aznar-Sánchez et al., 2020). In this context, biomass is projected to play an important role in meeting the global climate targets set in the Paris agreement (Stegmann et al., 2020). Cascaded crop residues and manures were able to prove their potential to increase the carbon content of soils and thus their ability to reduce greenhouse gases in long-term experiments (Bolinder et al., 2020).

There are many ways to return plant residues to the soil, ranging from ploughing standing crops or crop residues, incorporating crop residues directly or after a fermentation step (like composts or biogas fermentation of residues), or to spread solid and liquid manures (Davis and Abbott, 2006). However, maintaining crop material cycles in close spatial settings of the place of primary crop production and the incorporation of resulting residues also involves risks. While the associated phytosanitary risks are largely known and can be managed by crop rotation (Ratnadass et al., 2012) or residue processing (Termorshuizen et al., 2005), plant-born toxic organic compounds can be a challenge and might cause problems down the road for the agricultural sector but also for authorities or enterprises that maintain public lands, parks and greenery, on how to handle these residues correctly.

Recent studies indicated that toxic pyrrolizidine alkaloids (PA) of plant residues which are brought back to the fields can leach out into the soil and subsequently can be transferred and taken-up by succeeding non-PA crops farmed on this soil (Yahyazadeh et al., 2017; Selmar et al., 2019). PAs are a group of naturally occurring, plant exclusive alkaloids acting as defense compounds against herbivores. To date, more than 600 PAs and corresponding PA-N-oxides (PANOs) have been identified in over 6000 plant species (Hartmann and Witte, 1995; Smith and Culvenor, 1981).

PAs are well known hepatotoxic, genotoxic and carcinogenic compounds (Fu et al., 2004) and are recognized as natural contaminants in food and feed, thus posing a considerable health risk to humans and livestock (Alexander et al., 2011; Moreira et al., 2018). The toxicological mode of action of PAs/PANOs is well studied, and two basic structural prerequisites (1,2-unsaturation in the necine base part of the molecule and esterification at the C-7 and/or C-9 position) need to be present for toxic effects (Fu et al., 2004; Alexander et al., 2011). These basic structural features for PA-toxicity are highlighted in Fig. 1 by grey circles and C-atom numbering. Recent investigations have demonstrated that the occurrence of PAs in herbal products was mainly caused by co-harvesting PA-containing weeds together with the non-PA target crops resulting in PA levels of concern in food and/or feed (Bodi et al., 2014).

Currently, there are only a few PA-plants used for commercial production, mainly from the Boraginaceae plant family known for high-quality health beneficial seed oils, like Borago officinalis (Navarro-Herrera et al., 2018), Buglossoides arvensis (Lefort et al., 2016), Echium plantagineum (Kitessa et al., 2011), or Lappula squarrosa (Cramer et al., 2014). In contrast to PA-weeds, those cultivations generate considerable amounts of production residues, which might cause problems in the long term if such PA contaminated residues (e.g. from oil production) remain or go back to the fields. In addition, for some other plant species in our region, mainly from the Asteraceae family (tribe Senecioneae), it is observed that some species like Senecio jacobaea (syn.: Jacobaea vulgaris), Senecio aquaticus (Chizzola et al., 2019; Zacharias, 2018), or the neophyte to European areas Senecio inaequidens (Eller and Chizzola, 2016), may mass-infest pasture areas or public land (parks, greenery, nature preserves and ancillary areas of transport routes/road sides) (Lattrell, 2015). Those cuttings and green wastes naturally contain a high load of toxic PAs/PANOs that needs to be dealt with.

Hence, the possible carry-over of PAs from PA-plant matter due to closed-loop cycling via soil to the next generation crops farmed on this soil was the trigger to investigate the potential of possible pre-treatments. The extent to which the processing of plant residues before their return as organic soil fertilizer offers the opportunity to degrade PAs has hardly been investigated so far.

Previous studies have demonstrated the stability of PAs in dried plant matter like hay or herbal teas over months (Kaltner et al., 2018; Mädge et al., 2015) and to a lower extent also for silage (Gottschalk et al., 2015).

This study was intended to provide data on PA-degradation during composting and biogas fermentation as the two most relevant biochemical conversion procedures in practice. The aim was to evaluate the possibilities of such treatments to reduce the amount of the poisonous PA contents of the initial plant feedstock. Two model systems were chosen to cover the most obvious scenarios of possible PA-transfer in farming: a) residues from commercially grown Boraginaceae species (here: L. squarrosa) and b) residues from frequently occurring massive invasions of Senecio spp. (here: Senecio jacobaea) of public areas or extensively used grasslands. These two model systems also cover the two main classes of PA-structures: cyclic diester PAs (Senecio spp.) and open chain monoesters (Boraginaceae) (Fig. 1). Both are the key compounds which were in the focus of the contamination of the food and feed chains in the last decade (Mulder et al., 2018). Moreover, the study aimed at evaluating whether PA-plant residues can be channeled back into closed-loop farming, without risking the contamination of next season crop production and the biological/commercial utilization of those treatments.

Section snippets

Plant materials

Above ground parts of S. jacobaea were harvested locally at peak flowering stage (BBCH stage 57 according to Meier (2001)). For compost experiments, plants were collected in July 2018 and 2019 in the vicinity of Braunschweig (Germany) and accordingly for the biomethanization experiments in the vicinity of Rostock (Germany) in 2019, respectively. For composts, the fresh above ground plant material was harvested and manually cut into segments of about 100 mm length, mixed until homogeneity and

Results and discussion

Two possible routes for the treatment of PA-contaminated plant material were investigated in this study. While the L. squarrosa press cake used for the experiments was identical in all experiments, the Senecio-experiments required fresh plant material of S. jacobaea. Each year, the plant material was collected locally at its peak of flowering. To generate a broader picture, in terms of replicates, the composting procedure was conducted in two consecutive growing seasons (2018 and 2019) to cover

Conclusion

In this study, composting and wet fermentation for biogas production were tested with regard to their capability to degrade toxic pyrrolizidine alkaloids in plant biomass feedstocks.

By applying a sum parameter method for the detection and quantification of toxic PA structures (this means: all 1,2-unsaturated retronecine- and heliotridine-type ester PAs), we were able to cover and include unexpected toxic PA-like structures as well. Besides the common PAs and PANOs of the starting PA-plant

Author contributions

Mohammad Said Chmit: Methodology field survey, Methodology analytical work, Investigation, Data curation field data, Data curation laboratory data, Formal analysis, Writing – original draft, Writing – review & editing, Project administration. Jürgen Müller: Conceptualization, Investigation, Application of statistical, Data curation field data, Writing – review & editing. Denny Wiedow: Investigation, Laboratory experiments, Writing – review & editing. Gert Horn: Methodology field survey,

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

M.S. Chmit thanks the Niedersächsisches Ministerium für Wissenschaft und Kultur for the scholarship within the framework of Wissenschaft. Niedersachsen.Weltoffen.

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