Staphylococcus argenteus: an emerging foodborne pathogen?

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ScienceDirect Staphylococcus argenteus: an emerging foodborne pathogen? Xianming Shi and Dao-Feng Zhang Staphylococcus argenteus is an emerging species of the S. aureus complex (SAC) with increasing clinical importance and a global distribution. It is more and more clear that S. argenteus shares the majority of the S. aureus core and accessory genes, especially those encoding virulence determinants, of which the staphylococcal enterotoxins (SEs) are a major cause of foodborne illnesses, and were previously thought to be mainly produced by S. aureus. Recently, the causative pathogen in three food intoxication cases in Japan was found to be S. argenteus. Current knowledge indicates that S. argenteus may thus be as a foodborne pathogen. Here, we review the advances in knowledge on S. argenteus with highlights on its potential hazard for food consumers. Address MOST-USDA Joint Research Center for Food Safety, School of Agriculture and Biology & State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai 200240, China Corresponding author: Shi, Xianming ([email protected])

Current Opinion in Food Science 2018, 20:76–81 This review comes from a themed issue on Food microbiology Edited by Siyun Wang

https://doi.org/10.1016/j.cofs.2018.03.015 2214-7993/ã 2018 Published by Elsevier Ltd.

Introduction The coagulase-positive staphylococci (CoPS), especially Staphylococcus aureus, have been shown responsible for foodborne illnesses, induced by ingestion of their preformed staphylococcal enterotoxins (SEs) [1]. In 2015, two CoPS species, S. argenteus and S. schweitzeri, were proposed within the S. aureus complex (SAC), which were theretofore recognized as parts of S. aureus according to phenotype [2]. Recently, S. argenteus has been shown to have a global distribution and to be associated with serious morbidity and nosocomial infection. This species had spread in northern Australia and Thailand, but isolates were rarely recovered from other countries. To date, genome sequences from more than 100 isolates have been sequenced for S. argenteus according to NCBI data (Nov. 2017), and comparative genomics suggests that S. argenteus shares considerable amounts of the gene reservoir Current Opinion in Food Science 2018, 20:76–81

(including core and accessory genes) with S. aureus and S. schweitzeri [3,4]. However, significant divergence and rare recombination were also observed among their core genomes. Most recently, the causative microbe in three food intoxication incidents (2010, 2014 and 2015) in Japan were documented to be caused by S. argenteus [5,6]. According to the definition that a foodborne pathogen is responsible for food intoxication, toxicoinfection or foodborne infection [7], S. argenteus should be recognized as a foodborne pathogen for causing food intoxication. Here, we present a review of the recent explosion in knowledge on the virulence, distribution and evolution of S. argenteus, aiming to call this bacterium to the attention of the food safety field. S. schweitzeri also possesses many of the same SE genes as S. aureus, but most isolates are found in non-human primates and bats of sub-Saharan Africa [2,3]. It is still not clear why S. schweitzeri is incapable of residing and flourishing in human and human-associated environments, though it is more similar to S. aureus than is S. argenteus in some aspects, such as producing yellow colonies [2,3]. Nevertheless, S. schweitzeri seems to be far from causing human infections and threatening food safety, although some isolates were taken from healthy human subjects [8,9]. Therefore, S. schweitzeri will not be discussed in this review.

A brief history of S. argenteus S. argenteus has many similarities to S. aureus phenotypically and genotypically, and it is difficult to distinguish them using routine diagnostic microbiological identification methods [2,3,10,11]. S. argenteus isolates were often identified as a special lineage of S. aureus in earlier times, and the best way to rehabilitate these strains is to reevaluate their multilocus sequence typing (MLST) and genome data, because of apparent divergence among their core genomes [3,12]. MLST was established for S. aureus in 2000 [13], and it was followed by the earliest S. argenteus isolate of sequence type 75 (ST75) that we could track, in Australia, 2002 [14]. Subsequently, related STs (formed clonal complex [CC] 75) and isolates were reported in several other regions of Australia and other countries of the world (Table 1). A single-nucleotide polymorphism (SNP) genotyping system based on the MLST database was also used to some extent to investigate ST75-related isolates, though this method could not give a decisive ST [15–19]. Up to now (Nov. 2017), S. argenteus has been reported in 20 countries across the world (Table 1). Although MLST is a useful tool to determine the genetic structure of S. aureus, there were difficulties in applying www.sciencedirect.com

Staphylococcus argenteus: an foodborne pathogen? Shi and Zhang 77

Table 1 A brief history of the isolation of S. argenteus. Report year and location

MRSA

pvl

ST75*

R

ND

2

ST75* and ST258*

R

2004

72

ND

R

2003–2004

9#

ST75*

R

Human nares

2005–2006

2

ST1223

ND

Hospital Hospital Human nares

2006– 2003–2008 2006–2008

25 19 43

ND ST75* and ST883* ST1223

R/S R ND

[16] [22] [23]

Hospital

2003–

126#

ST1223, ST1823, ST1824, ST1848, ST1849 and ST1850

ND

[12]

Hospital Hospital and human nares Hospital Hospital

ND 2007–2008

9 6

ST2250 ND

S ND

2006–2007 2012

11 7

ND ND

S S

ND

ND

6#

ND

ND

[2]

Hospital Hospital Hospital

2014 ND 2006–2007

2 1 10

ND ND ND

+ ND

[25] [26] [27]

United States 2016 Belgium Gabon Northeast Thailand

Hospital

2012–2013

1

ST1223, ST1850, ST2198, ST2250, and ST2793 ST2250 ST2250 ST1223, ST2198, ST2250 and ST2854 ST2250

Healthy human Feces of gorilla Hospital

2007–2014 2012 2010–2013

3 1 58

Shanghai and Ningbo, China 2017 Denmark

Hospital, healthy human and pork

2005–2014

6

Hospital

2013–

25

Hospital

2006–2013

78#

Feces of patients and food Hospital Nares of food handlers

2010–2015 2012–2014 2012–2014

2002 Australia 2004 Australia 2006 Australia

Australia 2009 Cambodia 2010 Australia Australia French Guiana 2011 Australia

2014 Denmark Fiji; New Zealand Fiji Trinidad and Tobago 2015 Australia; Fiji; United Kingdom France Singapore Thailand

France; Israel; Malaysia; Singapore; Thailand Japan Laos Myanmar

Resource

Isolation year

Isolates

Hospital

ND

1

Hospital

ND

Throat swabs of people with pyoderma Hospital

Lineages

Ref. [14] [20]

ND

[15]

[21] ND

ND ND

[10]

[24] [19] [17] [18]

S

[28]

ST2250 and ST3240 ST2198 ST1223, ST2198, ST2250 and ST2854 ST2250 and ST3261

R/S S S

[29] [30] [31]

S

[11]

R/S

[32]

3

ST1223, ST2250, ST2783 and ST2845 ST1223, ST2198, ST2250 and ST2854 ST1223

6 5

ST1223 and ST2250 ST2250

+/

S

+/

[4]

ND

ND

[5,6]

R/S ND

ND

[33] [34]

These reports were summarized based on tracking related STs and genomes of S. argenteus. The list excluded literature using only isolates reported prior to that. #, some of the isolates had been reported in previous works. *, these STs may contain mistakes in aroE locus; please see ‘A brief history of S. argenteus’ section for more information. ND, no data available; R, the isolates were methicillin-resistant (MRSA); S, the isolates were methicillinsusceptible (MSSA); +, positive for pvl detection; , negative for pvl detection.

the S. aureus MLST method to S. argenteus isolates. The aroE and glpf were the toughest gene loci to perform PCR amplification, and redesigned primers were used to overcome it [10,35]. Meanwhile, apparent divergence of seven MLST loci was observed between S. argenteus and S. aureus, as well as other housekeeping genes, gap, rpoB, www.sciencedirect.com

sodA, tuf, and hsp60 [35]. On the basis of these observations, Ng et al. [35] stated: ‘We consider it possible that the aroE alleles in CC75 sequence types ST75, ST850, ST883, and ST1304 in the MLST database are not correct and are due to the conjunction of primer template mismatches and PCR contamination.’ This conjecture seems Current Opinion in Food Science 2018, 20:76–81

78 Food microbiology

to be reasonable, since isolates assigned to these STs were not reported in Australia after that, nor in any other country. Recently, a portable PCR-based method targeting a hypothetical nonribosomal peptide synthetase (NRPS) gene was developed to differentiate S. argenteus from S. aureus [11].

Table 2 SE gene profiles among SAC species. Species S. aureus

S. argenteus

Holt et al. [12] reported the first genome of S. argenteus (strain MSHR1132) in 2011, and suggested that: the 16S rRNA gene was identical between MSHR1132 and S. aureus; approximately sevenfold greater divergence between orthologous genes in S. argenteus and typical S. aureus than that observed within S. aureus; many genetic elements on accessory genome of S. aureus were found in S. argenteus, including vSAa, vSab, SCCmec, and plasmids; lack of the operon crtOPQMN for production of staphyloxanthin responsible for the characteristic golden color of S. aureus. These results called for serious consideration for recognition of CC75-related lineages as a new species, named S. argenteus [12]. In 2015, S. argenteus received formal taxonomic classification [2], and this rearrangement in SAC was subsequently introduced to clinical microbiologists [36]. Since then, there are increasing reports on S. argenteus presence in other countries (Table 1). In 2017, comparative genomics showed that there was no difference in virulence gene contents between S. argenteus and S. aureus, and population structure indicated distinct genetic backgrounds and rare recombination between the two core genomes [3]. Genome epidemiology suggested that S. argenteus ST2250 emerged in Thailand an estimated 15 years ago and that international spread of S. argenteus has occurred [3,4].

Virulence potential of S. argenteus So far, most known S. argenteus isolates were recovered from human infectious lesions and asymptomatic carriers. Some isolates belong to methicillin-resistant SAC (MRSA), and some harbor genes coding Panton-Valentine leukocidin (PVL) (Table 1). Several reports suggested that S. argenteus could cause clinical disease similar to that of S. aureus, including skin and soft tissue infection, abscess, bacteremia, pneumonia, sepsis, bone and joint infections, and even death [16,27,31]. S. argenteus has been equipped with the homologs of all virulence genes expressing the essential functions required for the pathogenicity in S. aureus, including icaA-D which encodes polysaccharide biosynthesis (critical to biofilm elaboration), esaA-C, essA-C, and esxAB for the ESAT-6 system (VII secretory system), isdA-G and srtB for heme uptake, and the genomic islands vSaa and vSab carrying many virulence determining genes [3]. Most of the virulence genes absent in S. argenteus encode for enterotoxins and exotoxins, which are usually located in mobile elements and easily acquired or lost [3]. Of the greatest interest for this review, the SE genes are summarized in Table 2, and half of them were found in S. argenteus. Current Opinion in Food Science 2018, 20:76–81

S. schweitzeri

SE genes sea, seb, sec, sed, see, seg, seh, sei, sej, selk, sell, selm, seln, selo, selp, selq, ser, ses set, selu, selv, selw, selx, sely, selz, sel26, sel27 seb, seg, seh, sei, selm, seln, selo, selu, selx, sely, sel26, sel27 seb, seg, sei, sell, selm, seln, selo, selu, selx, sely, sel26, sel27

The results were summarized based on two previous reports [3,37].

Nowadays, the most prevalent lineages of S. argenteus are ST2250 and ST1223: ST2250 present in 13 of the 20 countries with reported S. argenteus while ST1223 present in seven, excluding those countries with S. argenteus of undetermined STs (Table 1). The two lineages both have clinical importance and can reside in healthy humans. Dramatically, of the more broadly distributed lineage, ST2250 was found to only possess four SE genes, selx, sely, sel26 and sel27 [3,4], while the SE genes should play an important role in the pathogenicity [1,38]. The selx is located in the core genome of SAC [39]. The sel26 and sel27 were previously reported as entQ and secbov, respectively, specific to ST2250 lineage [4], but it was recently suggested that they represent two novel SE types present upstream of some subtypes of vSab genomic island among all three SAC species [37]. ST1223 showed lower a level of virulence than ST2250 in clinical practice (Table 1), but is currently the only lineage causing foodborne illnesses [5,6]. ST1223 possesses many more SE genes than ST2250, including seb, ‘seg’ (pseudogene), sei, selm, seln, selo, selu and selx, but the agent responsible for food intoxication was shown to be seb [3,5,6]. The ‘seg’ (pseudogene), sei, selm, seln, selo and selu also form an enterotoxin gene cluster (egc) in S. argenteus ST1223 the same as in some S. aureus lineages, while apparent differentiation (4–15%) was observed at each gene locus between the two species [3,6]. According to the proposed cutoff (10%) of the SE classification standard [40], some alleles of the egc genes from different species might be assigned to different SE types. Nevertheless, the seb alleles from S. argenteus and S. aureus shared high nucleotide sequence similarity (>97%) [3].

The original habitat of S. argenteus is still unclear A notable phenomenon is that S. argenteus was rarely isolated in most regions after its taxonomic establishment, though many researchers were well informed on this new species. It should not be overlooked that existing reports are mainly from clinical microbiologists and the isolation resources of screened bacterial collections were mainly human healthcare-associated. In a previous report, we screened a collection of purported ‘S. aureus isolates’ from food samples, and only one isolate from pork was www.sciencedirect.com

Staphylococcus argenteus: an foodborne pathogen? Shi and Zhang 79

determined as S. argenteus [11]. Therefore, it is reasonable to suspect that the original ecological niche of S. argenteus has not been determined, but S. argenteus is not primarily a human pathogen. Here, we support the hypothesis that S. argenteus came from livestock-associated environments and the dominant lineages, especially ST2250 and ST1223, have undergone host adaptation [3,4,11]. The supporting information is implied by specific genes on ST2250 genomes. Firstly, sel26 and sel27 were rarely present in S. aureus, but we found that three of four S. aureus isolates (screened from 248) harboring the two genes were isolated from raw milk [37]. These two genes might thus be livestock-associated. Secondly, clustered regularly interspaced short palindromic repeatsassociated (CRISPR-Cas) system, tetracycline resistance gene tet(L) and heavy metal resistance-encoding genes were mainly reported in livestock-associated S. aureus isolates [4]. Additionally, we found that the operon crtOPQMN was also absent in the genome of S. aureus subsp. anaerobius (ANIT00000000), which produces white colonies and is characterized by chronic subcutaneous abscesses near superficial lymph nodes in sheep and goat [41]. On the basis of this hypothesis, the hazard of S. argenteus to livestock-associated food products is possibly underreported and underestimated.

How to protect food products from S. argenteus The distribution of S. argenteus in food products is still unclear, since few studies have touched on this topic. Nevertheless, as stated above, S. argenteus has the virulence potential to threaten food safety and indeed has induced food intoxication in Japan. It is reasonable to suspect that S. argenteus has been contaminating food products, especially livestock-associated ones. However, for clinical isolates, the distributions of S. argenteus in food should differ among regions across the world. There is no need for S. argenteus to require different antimicrobial regimens from S. aureus, because it is actually more susceptible to antimicrobial drugs [31]. Considering the similarities of genotype and phenotype between S. argenteus and S. aureus [2,3], we suggest that a similar strategy as currently formulated for S. aureus could be used to control S. argenteus. This comes two aspects: control the factors influencing the growth, including water activity, pH, redox potential, temperature, nutritional factors and bacterial antagonism; detect the microbe and SEs, including molecular, immunological and mass spectrometry-based methods. The detailed practices for S. aureus were well-documented and readers are encouraged to refer to Hennekinne et al. [1]. However, there are apparent divergences of the core genome and many virulence genes between S. argenteus and S. aureus, and hence there is no guarantee when detecting some genes of S. argenteus using the methods developed for S. aureus. Additionally, the variants of some SE between the two species diverge to a considerable degree, so use of www.sciencedirect.com

some commercial products for detecting SEs by immunological methods may also be questionable.

Conclusion S. argenteus should be recognized as an emerging foodborne pathogen, while its prevalence and distribution in food products are still unclear. Livestock-associated environments are suspected habitats of S. argenteus, and more attention should be paid to livestock-associated food products in surveillance. Nevertheless, this conjecture needs to be clarified. Emergence of S. argenteus underscores the need to develop uniform methods for the detection of S. argenteus and S. aureus, and even S. schweitzeri, and to develop related typing methods. Differences in virulence between SE variants expressed by S. argenteus and S. aureus should also be clarified.

Conflict of interest None.

Acknowledgements We would like to thank Professor Harold Corke for English language editing of the manuscript. This study was supported by the National Key R&D Program of China (grant number 2016YFE0106100) and the National Natural Science Foundation of China (grant number 31671943). The funding bodies played no role in the preparation of the manuscript.

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