Folia Microbiol DOI 10.1007/s12223-013-0299-6

Laribacter hongkongensis: an emerging pathogen of infectious diarrhea M Krishna Raja & Asit Ranjan Ghosh

Received: 17 June 2013 / Accepted: 27 December 2013 # Institute of Microbiology, Academy of Sciences of the Czech Republic, v.v.i. 2014

Abstract Laribacter hongkongensis is relatively a new name in the list of bacterial pathogens for gastroenteritis and travelers’ diarrhea. Addition of another name increases burden on the enteric infections as a whole. L. hongkongensis belongs to Neisseriaceae family of β subclass Proteobacteria. L. hongkongensis was initially isolated in Hong Kong from blood and empyema of an alcoholic cirrhotic patient in 2001, followed by reports from Korea and China, representing a total of 38 articles in PubMed until April 2013. As of now, there is no report from Indian subcontinent where infectious diarrhea is very much prevalent and a major burden. This review provides information about the microbiological characteristics, consideration of an emerging pathogen, relative pathogenicity, genome and proteome content, resistance toward multiple antibiotics, adaptability to different stress, and other features since its time of discovery. Investigation for this bacterium may avoid misidentification as other microbial flora. Further studies like the geographical distribution, type of infection, disease burden, pathogenicity, or genomic exploration of this bacterium will be useful in characterizing them properly. This bacterium may possibly be the emerging threat to public health.

Introduction Gastrointestinal infection is one of the common episodes among Asian and African populations. The range and burden of infectious diseases are enormous and more prominent and menacing. Gastroenteritis is the disease resulting in 1.8 million deaths in children a year, with most of them in the world’s M. K. Raja : A. R. Ghosh (*) Centre for Infectious Diseases and Control, School of Bio Sciences and Technology, VIT University, Vellore 632014, India e-mail: [email protected]

developing nations including India (Bryce et al. 2005). Indian infants suffer and share larger proportion globally leading to diarrheal death (Ghosh et al. 1992). The list of diarrheagenic pathogens including virus, bacteria, fungi, and protozoa is long and distributed globally. Again, novel pathogens are emerging and old pathogens are reemerging with reprisal consequently and increasing challenges against known infectious Escherichia coli (Paul et al. 1994), Vibrio spp. (Ghosh and Sehgal 1998), and other diarrheal agents in gastroenteritis. It is a fact that no method so far has been described and discovered to isolate 100 % pathogens from hospitalized diarrheic patients. The recovery rate is somewhat improved with the introduction of molecular biology tools but could not reach to complete identification. Because of the inbuilt limitation of the peripheral and central laboratories in our hospital setting, the isolation of diarrheagenic bacteria remains restricted to the pathogens of endemic or/and pandemic potential. Referral laboratories are also not able to examine all the possible pathogens from clinical samples. Thus, in this situation and in most of the time, emerged pathogens are undiagnosed with the conventional and biased diagnostic system and also remain deficient in complete diagnosis of known cases (Petti et al. 2005). When conventional methods fail, a better alternative method is evolved, as with the case of surveillance of unknown infectious agents by genome homology. A case of non-gastroenteritis became the source of an emerging pathogen for gastroenteritis following the strategy of genome homology. A group of scientist from Hong Kong isolated a bacterium from blood and empyema of a patient with alcoholic cirrhosis in 2001. The 16S rRNA typing grouped this bacterium under Neisseriaceae family of β subclass Proteobacteria. This newly isolated strain was named as Laribacter hongkongensis. Laribacter refers to seagull-shaped rod, while hongkongensis a tribute to its discovered province (Yuen et al. 2001). It was subsequently discovered from the stool of six patients

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including three Asians and three Europeans with communityacquired gastroenteritis in Hong Kong (Woo et al. 2003). Later on, a case-control study was conducted (Woo et al. 2004), which revealed the relationship between L. hongkongensis and community-acquired diarrhea with the consumption of fish and travel. In the course of time, L. hongkongensis was also isolated from the patient with gastroenteritis outside Hong Kong (Ni et al. 2007).

How to isolate and identify? L. hongkongensis is cultivable onto any basal media and MacConkey agar. On MacConkey, it grows as non-lactosefermenting colony. Gram staining shows negative reaction with seagull-shaped appearance. The cultivability of L. hongkongensis onto MacConkey agar with an antibiotic, coupled with biochemical tests like catalase, cytochrome oxidase, arginine dihydrolase, and urease may help to isolate and identify this pathogen presumptively (Table 1). Sharing of similar seagull shape with Campylobacter can also be differentiated through aero tolerance testing (Woo et al. 2003). However, conventional phenotypic and other biochemical assays are not accurate in identifying this bacterium even by using commercially available phenotypic identification systems, like Vitek GNI, API 20E, and/or API 20NE, respectively. Thus, this remains the major obstacle in evaluating the prevalence, estimating pathogenic potential, and epidemiology of L. hongkongensis. Due to this constrains, initially identified Acinetobacter iwoffii by conventional identification methods was later identified as L. hongkongensis by molecular methods (Kim et al. 2011). It, therefore, requires the use of molecular biology tools for proper identification. Apart from 16S rRNA gene, species-specific duplex PCR assay, 16S-23S rRNA intergenic spacer region (Shen et al. 2011) and matrix-assisted laser desorption ionization time of flight mass spectrometry have also been used for identification (Tang et al. 2013). The 16S rRNA analysis figured out 6.2 % base difference with Microvirgula aerodenitrificans, 7.7 % with Vogesella indigofera, and 8.2 % with Chromobacterium species which made them to be grouped under proteobacter classification (Yuen et al. 2001). L. hongkongensis type strain HKU1 has 68.0±2.43 % by mole of G + C content on their total 3 Mb genome size (Yuen et al. 2001). Other strains of L. hongkongensis have also been isolated from different sources including human, fish, frog, water bird, and water, using 16S rRNA analysis (Yuen et al. 2001; Teng et al. 2005; Lau et al. 2007, 2009a; Ni et al. 2011). It was difficult to isolate the novel bacterium from diverse clinical and environmental samples using a battery of conventional media at different conditions. However, a selective medium was designed and successfully developed for selective isolation of L. hongkongensis. The designed selective

Table 1 Characteristics of L. hongkongensis (Yuen et al. 2001; Lau et al. 2003) Classification

Neisseriaceae family—β subclass Proteobacteria—Laribacter hongkongensis

0.79 to 2.5 μm size, gram-negative rod (seagull shaped), facultative anaerobe, motile (with tufted bipolar flagella or aflagellated), non-sporulating, nonfermentative Positive biochemical tests Catalase, cytochrome oxidase, nitrate reduction, arginine dihydrolase, and erease Selective medium Cefoperazone containing MacConkey agar Growth condition 37 °C for 48 h at aerobic condition Expected colonies onto Lactose-negative colonies MacConkey medium Phenotype

medium was MacConkey agar supplemented with 32 μg/mL cefoperazone, named as cefoperazone MacConkey agar (Lau et al. 2003). However, the concentration between 32 and 16 μg/mL of cefoperazone can also be used as selective medium (Ni et al. 2007).

Epidemiological importance While reviewing the impact of L. hongkongensis to the humans since the first report, stool samples of six diarrheic patients were analyzed: three from Hong Kong and three from Switzerland (Woo et al. 2003). Among the six samples, there was no known and expected pathogen like Salmonella spp., Shigella spp., enterohemorrhagic E. coli, Vibrio spp., Aeromonas spp., Plesiomonas spp., or even Campylobacter spp. Additionally, other analysis like electron microscopic examination for viruses, rotavirus antigen detection, and microscopic examinations for ova and cysts also showed negative (Woo et al. 2003). The 16s rRNA typing confirmed the presence of L. hongkongensis. Among three patients from Switzerland, one was a baby boy of 1 year old and thus, this showed that L. hongkongensis infects infants too. The type strain HKU1 first isolated from blood is flagellated, while other isolates from stools were motile with bipolar flagellates. The maximum base pair difference among six strains from stool and comparing with the type strain HKU1 was just 0–2 base pairs but the SpeI-digested genomic DNA on pulsed field gel electrophoresis (PFGE) revealed that all isolates were unrelated in their genotypes (Woo et al. 2003). After detailed food surveillance, the major source of the infection was identified to be the fresh water carp varieties of fishes and edible frogs (Teng et al. 2005; Lau et al. 2009a). The hunt for L. hongkongensis continued, and all isolates were PFGE analyzed and ribotyped. The disease prevalence and burden of the infection due to L. hongkongensis assessing the

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morbidity, mortality, or/and DALY (disability adjusted life year) was not enough from the reported research articles.

Ecosystem and transmission The fish species listed (Fig. 1) being the major reservoir of this bacterium (Teng et al. 2005) transmits to the surrounding environment plausibly by contact or through consumption. This organism might not be a contaminant to the carp varieties of fish, rather an autochthonous member of intestine, as L. hongkongensis was isolated from intestines of fish and frogs from retail markets (Feng et al. 2012). Moreover, expression pattern of argB-20 and argB-37 at different temperatures support the adaptability of L. hongkongensis to different hosts (Woo et al. 2009). The ecosystem is specific toward fresh water as L. hongkongensis is absent in marine sources. The sketch does not include other components of pond ecosystem as those are not the preferred host of this bacterium as of now. Fowls like duck, goose which have direct relation with this ecosystem, and others including chicken and mammals like cow and pig do not show positive for L. hongkongensis in their fecal swabs (Teng et al. 2005). L. hongkongensis thus appeared to exist in the human food chain (water, fish, frog, etc.).

Pathogenicity In general, a pathogenic microbe must possess certain essential features. Specifically for gastroenteritis causing bacterium, it must adapt to the acidic gut environment, resist to bile salts, capable to adhere the intestinal linings, colonize, and have the ability to compete with existing microbes of gut and to produce toxins or/and to invade the host-cell system. Adaptation to hosts Genomes encode all the information about the organism either their adaptive or resistance to different host. As described earlier, the genome possesses the typical genes for gut environment like acid resistance, adhesions for colonization of intestinal mucosa, catalase activity, bile salts efflux pump, and urease cassette (Woo et al. 2009). For acid resistance, L. hongkongensis has similar mechanism of urease activation like other diarrheal pathogens (Lau et al. 2011b). The histidine residues at the carboxyl terminal of UreE, an accessory protein, might bind to the nickel ions that are transported through a nickel transporter and donate them to UreC, a structural protein, during urease activation (Lau et al. 2011b). Host defense is violated through catalase and putative superoxide dismutase by resisting hydrogen peroxide and superoxide radicals generated by neutrophils.

The availability of information about the proteome and genome of one of the L. hongkongensis strains HLHK9 (Woo et al. 2009) provides clues for understanding their adaptability toward 37 °C (human) and 20 °C (fish, water). With regard to proteome for adapting different temperature because of the different hosts, the expression levels of the genes argB, argB-20, and argB-37, which encode two isoenzymes of N-acetyl-L-glutamate kinase, NAGK-20 and NAGK37, show higher expression at 20 and 37 °C, respectively in the arginine biosynthesis pathway (Woo et al. 2009). This organism survives both the aerobic and anaerobic conditions by selecting the right electron acceptors. Three terminal cytochrome oxidases opt for oxygen during aerobic and utilize reductases like dimethylsulfoxide (DMSO) reductase, fumarate reductase, nitrate reductase, and tetrathionate reductase for anaerobic respiration (Woo et al. 2009). Virulence The ability of this bacterium to adapt different hosts like humans, fish, frog, water bird, and yet the undiscovered host indicates its quick transmission and ability to survive in multiple hosts. This feature also made us think if it does undergo constant mutation or constantly changing the expression profile. Virulence nature of L. hongkongensis includes autoaggregation, biofilm formation, invasion, and cytotoxicity (Woo et al. 2009). Virulence factors like collagenases, cytotoxins, hemolysins, RTX toxins, lipopolysaccharides, patatinlike proteins, and phospholipase A1 also contribute for pathogenecity (Woo et al. 2009). Clustering of groups in PFGE and in multi-locus sequence typing (MLST), the incongruence in the pairwise comparisons among seven MLST loci indicates that recombination might occur to lead to the evolution of L. hongkongensis, resulting in more clonal and virulence strains (Lau et al. 2010; Teng et al. 2005). L. hongkongensis is included as a new agent associated with acute diarrhea along with enterotoxigenic Bacteroides fragilis and Klebsiella oxytoca (Marcos and DuPont 2007). Increase in heterogeneous population of this bacterium alarms the virulence and chance of contamination through water (Lau et al. 2007), fresh water fishes, and chance of being endemic. The most closely related species Chromobacterium violaceum and L. hongkongensis possess higher proportion of genes with putative functions related to signal transduction mechanisms. Neisseria meningitidis and Neisseria gonorrhoeae the senior members of this family are aerobic with humans as the only host; L. hongkongensis may carry the essential genes to adapt in multiple hosts and more specifically toward human. Transporters L. hongkongensis is not an exception in possessing seven major categories of transporters as detailed in Transporter

Folia Microbiol Fig. 1 Representation of the hypothetical ecosystem and plausible transmission routes favoring L. hongkongensis to different hosts

Classification Database (TCDB) (Lau et al. 2011a). L. hongkongensis possess transporters and efflux pumps to overcome stress conditions (Table 2). Apart from multidrug efflux, detoxification by heavy metal transporters, genes encoding for the transport of hemin helps in utilizing exogenous siderophores, or host proteins for iron acquisition that also assists in adaptability to host environment (Lau et al. 2011a). Multidrug resistance “It is not the strongest of the species that survives or the most intelligent, but the one most responsive to change”—words of Charles Darwin, father of evolution still remain applicable even after centuries. The recent year’s transformation from natural selection to selection by anthropogenic activities happened which resulted in evolution of multidrug-resistant microbes. Multidrug resistance is one of the feathers added to the cap of pathogenic microbes. The resistivity nature of L. hongkongensis is vast as it resist to most of the β-lactams, including broad-spectrum penicillin and cephalosporin, but is susceptible to carbapenems (Lau et al. 2005), amoxicillinclavulanate, quinolones, and amino glycosides. Ampicillinsulbactam and ciprofloxacin also shows susceptibility (Lau et al. 2009b). It is not like that all the L. hongkongensis follow the same resistance and susceptibility patterns, it differs with the isolates. Various antimicrobial-resistance class I integron genes like dfrA1, dfrA14, dfrA17, dfrA32, aadA1, aadA2, aadA5, cmlA5, arr2, ereA, and orfC (Feng et al. 2011) and the presence of different family of proteins like resistance-nodulation-cell division (RND) family proteins, major facilitator superfamily (MFS), small multidrug resistance (SMR) family, multidrug and toxic compound extrusion (MATE) family, ATP-binding

cassette (ABC) superfamily, and other miscellaneous resistance genes help in the effectivity in multidrug resistance (Lau et al. 2011b). L. hongkongensis represents the first of its Neisseriaceae family in tetracycline and β-lactams resistance genes (Table 3). As reported on 2007, only four isolates, three from human and one from fish, were resistant toward tetracycline with MIC 128 mg/L and doxycycline with MIC 8–16 mg/L and had reduced susceptibility to minocycline with MIC 1– 4 mg/L. The resistivity gene tetR, the repressor gene, and tetA

Table 2 Effective genes and their roles in different stress conditions (Lau et al. 2011c; Yang et al. 2011; Lau et al. 2011a) Different stress

Method of adaptation/gene possessions

DNA repair and recombination

Putative homolog of alkaline exonuclease (LHK-Exo) and SSAP (LHK-Bet) proteins

Acid stress Alkaline stress

Urease gene cassette and two arc genes Six CDSs for transporters of the monovalent cation/proton antiporter-2 and NhaC Na+:H+ antiporter families Heavy metals acquisition Possessed CDSs for iron and nickel transport and tolerance and efflux pumps for other metals Temperature stress Chaperones and chaperonins, heat shock proteins, and cold shock proteins Osmotic stress Potassium ion, proline, and glutamate transport Oxidative and UV light Oxidant-resistant dehydratase, superoxide stress scavenging, hydrogen peroxide scavenging Other adaptive Exclusion and export of redox-cycling processes/genes antibiotics, redox balancing, reduction of disulfide bonds, limitation of iron availability and reduction of iron-sulfur clusters, chemotaxis. Prophages, transposases, transporters

Folia Microbiol Table 3 List of genome and proteome information in different databases and their respective accession number (Woo et al. 2009; Yuen et al. 2001; Woo et al. 2007b; Lau et al. 2008; Lau et al. 2005; Yang et al. 2011) Strain/Gene name

Database

Accession number

Complete genome of HLHK9 16S rRNA gene sequence of HKU1 pHLHK26 pHLHK22 blaCLHK-1 blaCLHK-2 blaCLHK-3 blaCLHK-4 blaCLHK-5 blaCLHK-6 blaCLHK-7 tetALHK-5 Putative IS1341 element transposase Putative IS200 element transposase Crystal structure of LHK-Exo Crystal structure of LHK-Exo:dAMP complex Crystal structure of LHK-Exo:ssDNA complex Sequenced strain numbersa

GenBank sequence

CP001154

GenBank sequence

AF389085

GenBank sequence GenBank sequence GenBank sequence GenBank sequence GenBank sequence GenBank sequence GenBank sequence GenBank sequence GenBank sequence GenBank sequence GenBank sequence

DQ341277 EF679779 AY632070 AY632071 AY632072 AY632073 AY632074 AY632075 AY632076 AY903253 AAR96031

GenBank sequence

AAR96032

a

RCSB Protein Data Bank 3SYY RCSB Protein Data Bank 3SZ4

RCSB Protein Data Bank 3SZ5

StrainInfo

CCUG 45813, CIP 107139, DSM 14985, HKU1, LMG 21516, Yuen HKU1

http://www.straininfo.net/strains/330655

may be due to recombination, horizontal gene transfer, or through transposons (Lau et al. 2008). Gene tetA shows identity to transposon Tn1721 and also common among plasmids of other gram-negative bacterium (Lau et al. 2008). The other identical feature of tetA of HLHK5 strain is similar in sequence region with tetC of Chlamydia suis. The chromosome encoded Class C β-lactamase gene of L. hongkongensis HLHK5 strain showed differences with the conventional β-lactamase ampC gene by deletion of two amino acids in HKU1 and one amino acid in HLHK2 strains (Lau et al. 2005). On comparing the amino acid sequence homology with the known β-lactamase the closest similarity is 46 % with S. meliloti. L. hongkongensis ampC gene also contains the characteristic amino acid residues of serine β-lactamase. Moreover this bacterium is the first to represent the β-proteobacter subdivision with class C β-lactamase, with ampR the repressor regulating ampC (Lau et al. 2005).

Extra chromosomal DNA features In addition to the chromosomal DNA, several strains like L. hongkongensis HLHK26 and HLHK22 carry their own theta plasmids. Table 4 explains their size, group, and respective genes coding for. Possession of plasmids to L. hongkongensis is an extra feature to its better survival. Other plasmid size varies from 3 kb to more than 20 kb (Woo et al. 2007a). Other genes specific to HLHK22 includes tetA and tetR, the tetracycline-resistance genes. There are additional gene codes for putative acetyl transferase, RelE/StbE, addiction module toxin, MobB and MobA, conjugal transfer protein TrbJ, and KfrA protein (Lau et al. 2008).

Metabolism Outcome of genes through expression influences the metabolic pathway. The genome analysis of metabolic pathways for L. hongkongensis reveals that it lacks essential enzymes like glucokinase, 6-phosphofructokinase, and pyruvate kinase for glycolysis. Further, genes encoding for phosphoenolpyruvatedependent sugar-transporting phosphotransferase system is also deficient (Curreem et al. 2011). However, other essential pathways like gluconeogenesis, the pentose phosphate pathway, glyoxylate cycle, biosynthesis of the 21 genetically encoded amino acids, and β-oxidation of saturated fatty acids are complete with all enzymes. The occurrence of both the glutamate dehydrogenase and glutamate synthase pathways provide a clue that ammonia metabolism plays a vital role (Curreem et al. 2011). Being an asaccharolytic bacterium, the carbon source might be from amino acids or fatty acids or through transport of malate by C4-dicarboxylate family. Table 4 Comparative table for the well-studied plasmids of two different strains of L. hongkongensis (Woo et al. 2007b; Lau et al. 2008) Strains of L. hongkongensis Plasmid size Class

HLHK26

HLHK22

8.7 kb 15.6 kb Possibly of class A group Class A as it shares eight of the nine positions of the consensus DnaA box sequence of other class A plasmids Putative functions Putative plasmid partitioning TrbL/VirB6 plasmid protein conjugal transfer protein Putative ADP-ribose ATPase 1″-phosphatase activity Putative recombinase (TniR) DNA recombinase Putative replication protein Putative replication protein A

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Future investigations The possession of cryptic plasmid ORF with ADP-ribose 1″phosphatase, a ubiquitous enzyme is present in all three domains of living system. Another putative recombinase (TniR) of resolvase/invertase family shows high similarity in phylogenetic analysis with recombinase in a mercury-resistance plasmid of Sinorhizobium meliloti (Woo et al. 2007b). Reported articles disclose that this bacterium shares diverse genes of different bacteria and thus more genetic exploration is necessary. This will provide knowledge about different strains of this species and diversity. Analyzing the essential sequence tags can also be useful to understand the genetic makeup of different strains of this bacterium (Woo et al. 2010). Factors like ecology (seasonality), disease study models (Woo et al. 2005), epidemiology, and its diversity within different hosts can also be considered in analyzing severity and disease burden. With 2,091 transcription units, 1,246 enzymatic reactions, 70 transport reactions, 3,235 polypeptides, 207 pathways, 3 protein complexes, 873 enzymes, 108 transporters, and 892 compounds (Subhraveti et al. 2013), L. hongkongensis holds different ways of adaptability and possesses the capability to emerge as a pathogen.

Conclusion Diarrhea is predominant and a cause of socioeconomic burden in India. Along with known pathogens like E. coli, Shigella spp., Vibrio spp., Salmonella spp., Campylobacter spp., viruses, and parasites, L. hongkongensis would be a new challenge. However, molecular diagnostic approach would enable to reveal the disease burden due to L. hongkongensis in near future. Species-specific duplex PCR method can also be used as reliable alternative to conventional methods to identify L. hongkongensis in clinical and environmental samples (Shen et al. 2011). India being the world’s second largest producer of farmed fish, this bacterium may not be new to us. However, there is no report on isolation of L. hongkongensis in Indian subcontinents. This review might provide an insight about the emerging pathogen in near future. Acknowledgments Authors are grateful to the VIT management, VIT University, Vellore for pursuing the research.

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Laribacter hongkongensis: an emerging pathogen of infectious diarrhea.

Laribacter hongkongensis is relatively a new name in the list of bacterial pathogens for gastroenteritis and travelers' diarrhea. Addition of another ...
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