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Acta Agriculturae Scandinavica, Section B — Soil & Plant Science Volume 67, 2017 - Issue 6
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Original Articles

Caution of intensified spread of antibiotic resistance genes by inadvertent introduction of beneficial bacteria into soil

Yijun KangJiangsu Key Laboratory for Bioresources of Saline Soils, Yancheng Teachers University, Yancheng, P. R. China;College of Marine and Bio-engineering, Yancheng Teachers University, Yancheng, P. R. ChinaCorrespondence[email protected]
View further author information
,
Min ShenCollege of Marine and Bio-engineering, Yancheng Teachers University, Yancheng, P. R. ChinaView further author information
,
Dan XiaCollege of Marine and Bio-engineering, Yancheng Teachers University, Yancheng, P. R. ChinaView further author information
,
Kaixia YeCollege of Marine and Bio-engineering, Yancheng Teachers University, Yancheng, P. R. ChinaView further author information
,
Qingxin ZhaoCollege of Marine and Bio-engineering, Yancheng Teachers University, Yancheng, P. R. ChinaView further author information
&
Jian HuCollege of Environmental Science & Engineering, Yangzhou University, Yangzhou, P. R. ChinaView further author information
Pages 576-582 | Received 22 Feb 2017, Accepted 24 Feb 2017, Published online: 13 Apr 2017

ABSTRACT

The use of beneficial bacteria isolated especially from rhizosphere soils called plant growth-promoting rhizobacteria (PGPR) has been attracting particular interests. However, a potential source of antibiotic resistance genes (ARGs) carried by PGPRs and derived biocontrol agents and/or bio-fertilizers is widely forgotten and ignored. It is very urgent to raise the question if large-scale introduction of beneficial bacteria into soils can aggravate the situation in the spread of ARGs in environment. In this article, we conclude and analyze the possibility of a potential ARGs reservoir associated with introduction of PGPR strains into soils, and offer some advice on PGPR isolation, development and application.

Introduction

Since 1980s, the use of beneficial bacteria isolated especially from rhizosphere in agricultural process has been attracting particular interest because of their distinct advantages in low costs, environmental friendliness and enduring efficiency both for soils and plants (Bouis & Welch Citation2010; Kloepper et al. Citation1980). To date, a large number of bacterial strains, belonging to different genera including Pseudomonas, Bacillus, Paenibacillus, Serratia, Bradyrhizobium, Azospirillum, Acinetobacter, Alcaligenes, Enterobacter, Pantoae, Rhodococcus, Agrobacterium, Burkholderia, Gluconacetobacter, Achromobacter, etc. have been isolated and determined to be efficient in plant growth promotion and/or plant disease control (Beneduzi et al. Citation2013; Vessey Citation2003; Yuan et al. Citation2015), and thus called plant growth-promoting rhizobacteria (PGPR). However, in recent years, with the intensive studies in the spread of antibiotic resistance genes (ARGs) in environment with regard to their diverse transmission pathways (Lipsitch & Samore Citation2002), threats to human health and ecology (Martínez Citation2008), prevention and control measures (Spellberg et al. Citation2013), and so on, more and more people are beginning to worry about the negative impacts of inadvertent inputs of soil amendments containing ARGs sources, mainly referring to animal manures and with which some produced composts (Heuer et al. Citation2011; Zhu et al. Citation2013; Udikovic-Kolic et al. Citation2014; Kang et al. Citation2016), but a potential source of ARGs, PGPRs and derived biocontrol agents and/or bio-fertilizers, is widely forgotten and ignored. Based on the fact that maintaining critical population densities and better to be the dominant groups in soils is the precondition for many PGPRs in growth promotion (Cattelan et al. Citation1999; Kang et al. Citation2013), it is very urgent to raise the question if large-scale introduction of beneficial bacteria into soils can aggravate the situation in spread of ARGs in environment. In this paper, we conclude and analyze the possibility of a potential ARGs reservoir associated with introduction of PGPR strains into soils, and offer some advice on PGPR isolation, development and application.

A paradox behind use of wide adapted PGPRs and ARGs control

The unstable characteristics of many PGPR strains is a key limiting factor for large-scale use under different conditions, for they often lose competitiveness in ‘unfamiliar’ soils and cannot maintain critical population densities that, in many cases, are necessary for growth promotion (Cattelan et al. Citation1999; Kang et al. Citation2013). It is generally accepted that PGPRs with multiple stress resistance genes are adapted to diverse environments (Ma et al. Citation2016). For this reason, many researchers become more enthusiastic about screening resistant PGPRs for wide adaptation (Singh & Cameotra Citation2013; Wani & Khan Citation2013). Of which, for example, many strains of Bacillus sp. and Pseudomonas sp. are of plant growth-promoting potential and some of them have been used as microbial agents (Steil et al. Citation2003; Santoyo et al. Citation2012). However, many of these two genera are considered to have relatively abundant ARGs in soil (Gao et al. Citation2012; Wellington et al. Citation2013). Despite antibiotics resistance is hardly ever characteristic for screening of PGPRs in order to enhance survival abilities; many stress factors such as metals really represent co-selection mechanisms in prokaryotes (Baker-Austin et al. Citation2006). This becomes a paradox of using PGPRs avoiding introduction of excess ARGs into soil.

To what extent are there PGPRs with ARGs?

Based on the NCBI GenBank Database up to Dec 2016, a total of 31 genome-sequenced PGPR strains belonging to different subgroups were searched to reveal both chromosomal and plasmid-borne ARGs. As shown in , all listed strains contain more than one ARG and thus have multiple resistance profiles. Among which, almost every strain contains bac gene that confer the ability to resist bacitracin which are produced mainly by bacilli (Li et al. Citation2015). Due to the large population size of bacilli in soil, many bacteria like pseudomonas have to be resistant to bacitracin probably via some pathways such as horizontal gene transfer (HGT) (de la Cruz & Davies Citation2000).

Table 1. Antibiotics resistance genes and profiles of representative PGPR strains.

Some studies have showed that distinct tendencies of HGT events were found in different phyla of antibiotic-resistant bacteria (ARB). It is noted that ARGs are more prone to occur in Proteobacteria than in Bacteroidetes (Hu et al. Citation2013). Apart from Bacteroidetes that are too few to mention here, ARGs are really prevalent in Proteobacteria and Firmicutes. A probable hypothesis is that mobile elements containing ARGs predominantly originate from the phyla Bacteroidetes and Firmicutes based on phylogenetic analysis using PhyloPythia (McHardy et al. Citation2007; Sommer et al. Citation2010), from this point of view, using PGPRs of Firmicutes may result in increases of ARG reservoirs as donors, and aggravate the risks of spread of ARGs in soil. Certainly, introduction of large-scale PGPRs of Proteobacteria into the soil is not sensible either, for they could be additional acceptors for ARGs in soil and move towards plants more easily with pili that are often deficient in Firmicutes.

How to cope with the problem?

The possible ways to deal with the problem mentioned above are as follows:

  1. Apart from non-pathogenicity to plants, the resistance profiles of PGPRs and potential risks of spread of ARGs in PGPRs should be taken into account in the safety tests before large-scale application. PGPR strains with fewer ARGs can be used preferentially. Inoculation with PGPRs by spraying the leaves or by soaking seeds could mitigate the problem in soil.

  2. Metabolite production by PGPRs should give priority to using for plants promotion and/or biocontrol.

  3. Avoiding use of genetically engineered PGPRs with ARG biomarkers.

  4. Due to very few PGPR without ARGs in soil, those PGPRs with special ARG genotypes that do not occur in human gut microbiome should be forbidden.

Disclosure statement

No potential conflict of interest was reported by the authors.

Notes on contributors

Yijun Kang is an associate Professor at College of Marine and Bio-engineering, Yancheng Teachers University, Yancheng, Jiangsu, PR China, whose research interest focus on Agricultural/Environmental Microbiology.

Min Shen is a lecturer at College of Marine and Bio-engineering, Yancheng Teachers University,and her major is Environmental Microbiology.

Dan Xia and Kaixia Ye are postgraduate students at College of Marine and Bio-engineering, Yancheng Teachers University, and their major is Bioengineering.

Qingxin Zhao is a Professor at College of Marine and Bio-engineering, Yancheng Teachers University, and his research interest focus on Molecular Biology.

Jian Hu is a Professor at Environmental Science & Engineering, Yangzhou University, Yangzhou, Jiangsu, PR China, and his major is Agricultural/Environmental Microbiology.

Additional information

Funding

This work was supported by the National Natural Science Foundation of China [grant number 41501256] and [grant number 41101235], the Agricultural Innovation Project of Yancheng [grant number YK2015027], the ‘Qing Lan’ Project Foundation of Jiangsu Province, the 333 Talents Project of Jiangsu Province, and the Spark Plan [grant number 2015GA690257].

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