Flies as Vectors of Bacterial Pathogens: History
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Contributor:
Ji-Hang Yin
,
Patrick John Kelly
,
Chengming Wang

The unique biology of flies and their omnipresence in the environment of people and animals makes them ideal candidates to be important vectors of antimicrobial resistance genes. Consequently, there has been increasing research on the bacteria and antimicrobial resistance genes that are carried by flies and their role in the spread of resistance.

  • flies
  • bacterial pathogens
  • antimicrobial-resistance
  • sentinel
  • surveillance

1. Introduction

Flies are insects in the order Diptera that have one pair of wings for flight and a residual second pair of wings, known as knobs, which are used for balance [1]. Over 125,000 species of Dipterans have been identified, including gnats, midges, mosquitoes, leaf miners, horse flies, houseflies, blowflies, and fruit flies. Houseflies, Musca domestica Linnaeus (Diptera: Muscidae), are of particular importance as they are notorious “pests” that can transmit a variety of bacterial pathogens [2]. They are thought to have originated in the savannahs of Central Asia and later spread worldwide [3], particularly in tropical and subtropical areas where they are mostly associated with people and domestic animals in both rural and urban areas [4].
Flies have four life stages—eggs, larvae/maggots, pupae, and adults [5]. Female houseflies lay their eggs in compost, trash, soiled bedding, or manure containing moist and microbial-rich decaying organic matter near people’s houses and farms [2]. Each female can oviposit four to six times in her lifetime, each time producing 100–150 eggs [2][6]. The eggs usually hatch within 8–12 h if the environment is moist and at an optimal temperature of 25 °C to 30 °C [2]. The first-instar larvae feed on bacteria in nutrient-rich environments and pass through a further two instars before becoming larvae/maggots that migrate into a dark, dry, and cool place where they pupate [2][6]. Adult flies emerge around 2–4 days later when ambient temperatures are 32 °C to 37 °C, meaning the entire life cycle of houseflies is very rapid, ranging from 10–21 days [7].
The behavior of houseflies promotes their ability to transmit bacterial pathogens [8][9]. They live in close proximity to people (synanthropic) or in their dwellings (endophilic cosmopolitan), and they often feed on animal and human feces (coprophagic) and decaying matter, such as garbage [7]. All life stages can thus be exposed to a variety of pathogens in unsanitary environments, and these can then be mechanically transmitted to people [10]. Adult flies can move over distances of up to 20 miles in their lifetime, which means they are ubiquitous in the environment and well capable of disseminating pathogens from unsanitary areas into people’s homes and places of work and leisure [11].

2. Flies as Vectors of Bacterial Pathogens

Flies can carry a surprising diversity and number of pathogens. One systemic review revealed more than 130 human pathogens have been identified in houseflies [3], including bacteria, fungi, viruses, and parasites [3][12] The predominant pathogens are bacteria, including Klebsiella spp. [13], Salmonella [14], Pseudomonas aeruginosa [15], Campylobacter jejuni [16], Edwardisella spp. [17], Clostridium spp. [18], Yersinia enterocolitica [19], and Burkholderia pseudomalliei [20]. Recently, Balaraman et al. reported that houseflies acquired and harbored infectious SARS-CoV-2 for up to 24 h post-exposure. They could mechanically transmit SARS-CoV-2 genomic RNA to the surrounding environment for up to 24 h post-exposure [12].

2.1. External Carriage of Bacterial Pathogens

Flies have unique body structures that enable them to effectively carry bacteria. For example, bacteria readily become attached to the sticky leg pads, hairs, electrostatically charged exoskeleton, and sponging mouthparts of flies [8][21][22]. A study quantifying the transfer of fluorescence-labeled E. coli from sugar, milk, steak, and potato salad to houseflies revealed a single housefly can carry up to 2 × 1012 E. coli and approximately 0.1 mg of food between landing sites [23]. Flies were also found to externally carry Enterococcus faecium in poultry farms [24], Klebsiella pneumoniae in kitchens and farms [25], Salmonella enterica in swine farms [26], and Staphylococcus aureus in urban areas [19]. Female flies carry more bacteria than males because they visit oviposition sites that are heavily contaminated with bacteria [27].

2.2. Internal Carriage of Bacterial Pathogens

Although most studies have focused on bacteria carried on the body surface, some researchers have investigated bacteria carried internally within the digestive tract [28][29][30][31] Ingested material containing bacteria is initially stored in the crop, from where it passes down the digestive tract through the proventriculus/foregut, midgut, hindgut, and rectum [32]. Whereas epithelial cells in the foregut and hindgut are covered with a protective cuticle [33], the midgut is lined with a unique structure, named the “peritorphic matrix”, peritrophic envelope, or peritrophic membrane (PM) [29][34] (Figure 1). This is a double-layered, noncellular structure composed of chitin, proteoglycans, and various proteins [33] that serves as a physical barrier to prevent microbes in the ingesta from invading epithelial cells and causing damage [34][35]. The PM has gaps, ranging from 2 to 10 nm, which enable digestive enzymes, acid, and secretions to enter the endoperitrophic space and digest food materials [34][36]. At the same time, as part of an innate immune response, antimicrobial peptides, reactive oxygen species, and other epithelial secretions can enter the lumen and kill and digest the trapped bacteria [34]. Not all bacteria are killed, however, with species, such as Pseudomonas aeruginosa [28], Salmonella enterica serovar Typhimurium [29], and Aeromonas caviae [30][31], being able to be ingested and proliferate in the midgut before being shed in the feces in high numbers. The survival rate of ingested bacteria is dose-dependent [37] and also dependent on competition with the commensal microbiota [38]. Studies have shown that the numbers of pathogens in the digestive tract are three times higher than on the body surface, probably due to the multiplication of the pathogens in the digestive tract [39][40][41].
Vetsci 09 00300 g001 550
Figure 1. Fate of bacteria in the digestive tract (midgut) of flies. A: Ingested food with bacteria is predigested with saliva in the crop. The epithelial cells in the foregut are covered by a cuticle, which prevents bacterial invasion. B: In the midgut, digestion products can pass through gaps in the peritrophic membrane and enter the ectoperitrophic space to be absorbed by epithelial cells. C: Bacteria cannot pass through the gaps on the peritrophic membrane and remain in the endoperitrophic space. D: Bacteria are trapped in the endoperitrophic space, triggering an innate immune response in epithelial cells to produce reactive oxygen species (ROS) and antimicrobial peptides (AMP). E: Trapped bacteria are killed by ROS, AMP, pH changes, and digestive enzymes. F: Some bacteria survive in the hostile environment, pass through to the hindgut, and are shed. G: There might be horizontal gene transfer between bacteria surviving in the digestive tract and bacteria may be transmitted vertically to offspring.

This entry is adapted from the peer-reviewed paper 10.3390/vetsci9060300

References

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