Streptococcus bovis

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Streptococcus bovis, originally described as a single species, is a group of Gram-positive bacteria that is now known as the Streptococcus bovis Streptococcus equinus Complex. In humans, it is associated with urinary tract infections, endocarditis, sepsis, and colorectal cancer. S. bovis is commonly found in the alimentary tract of cattle, sheep, and other ruminants, and may cause ruminal acidosis. It is also associated with spontaneous bacterial peritonitis, a frequent complication occurring in patients affected by cirrhosis. Equivalence with Streptococcus equinus has been contested, with its classification under the Streptococcus bovis/Streptococcus equinus complex (SBSEC) in the late 1990s. [1]

Contents

Taxonomy and nomenclature

Historical use

Streptococcus bovis was a species that was discovered in 1919 by Sigurd Orla-Jensen from cow dung and milk. [2] It was studied as a distinct species and became a focus of research due to its link to endocarditis in the 1970's. [2] The species was divided into biotypes based upon biochemical characteristics until the later 1990's when the biotypes began to gain recognition as independent species. [2] [3] These biotypes were not recognized as individual species until 1984, when DNA-DNA hybridization showed that the biotypes were genetically distinct. [1] [2] The original taxonomy of S. bovis as an individual species began to be further investigated until the late 1990's and early 2000's when it became a term to describe the group of a new species that had once been called Streptococcus bovis.

Streptococcus bovis consisted of biotypes based upon biochemical characteristics. [4] Biotype I was distinguished based on the microbe's ability to ferment mannitol. Those that could not were separated into the Biotype II classification. However, this was further divided based on the ability to degrade bile-esculin, with those that could being distinguished as Biotype II/1, and those that could not as Biotype II/2.

S. bovis biotypes to SBSEC species and subspecies [4]
Original S. bovis BiotypeSBSEC Species and Subspecies Classification
Biotype IS. gallolyticus subsp. gallolyticus
Biotype II/1S. infantarius subsp. infantarius and S. lutetiensis
Biotype II/2S. gallolyticus subsp. pasteurianus

Streptococcus bovis Streptococcus equinus Complex (SBSEC)

When referencing S. bovis in current research, the term is often used within the Streptococcus bovis Streptococcus equinus Complex (SBSEC). [5] The SBSEC contains strains that were once classified as the species S. bovis, along with other closely related species. [4]

SBSEC Subspecies [5] [6]
Scientific Name
S. equinus
S. gallolyticus subsp. gallolyticus
S. gallolyticus subsp. pasteurianus
S. gallolyticus subsp. macedonicus
S. infantarius subsp. infantarius
S. lutetiensis
S. alactolyticus
S. ruminicola

Use of S. bovis in clinical practice

Despite the taxonomical changes that establishes the SBSEC as a group of species, rather than the single species S. bovis, in clinical practice, S. bovis is still used. Though subspeciation is important in appropriately understanding the connection to different conditions such as endocarditis and colorectal cancer (CRC), the frequent changes in taxonomy has made it difficult for clinicians to follow the appropriate terminology. [4] [7] [8] In addition, there are still developments in correctly identifying the individual species, which means S. bovis may still be used as an umbrella term in clinical literature, as the term is strongly associated with CRC. [9] [7] Research is needed in further differentiating these species, so that accurate epidemiological and clinical associations can be drawn to each species, contributing to understanding of their implications on human health. [7]

Microbiology of the SBSEC

Morphology and cellular characteristics

The Streptococcus bovis/Streptococcus equinus complex (SBSEC) consists of nonenterococcal, Lancefield group D streptococci. [10] Members of this group are Gram-positive cocci with a thick peptidoglycan wall containing teichoic acids and no outer membrane. [11] Their spherical or ovid-shaped cells grow as chains of cocci that divide along successive planes that are parallel to each other. [12] Chain lengths vary by culture conditions. In liquid culture, cells typically remain attached longer and form chains of varying length. On solid agar, cells separate more frequently, resulting in pairs or shorter chains of cells. [13] They are nonmotile, lack flagella, and do not form endospores. Surface structure vary among members, with some strains producing a le, and pilus types differing among species. [14]

Growth and physiology

SBSEC organisms are thermotolerant facultative anaerobes. They grow optimally at temperatures between 37-45°C with growth completely halting at extremes of 10°C and 50°C. They obtain energy primarily through carbohydrate fermentation, producing lactic acid as a major metabolic end product. [15] Members are catalase-negative and oxidase-negative, reflecting their lack of enzyme activity in biochemical tests. Organisms can grow in 40% bile salts but are typically intolerant to 6.5% NaCl solutions. [16]

Historical biochemical identification

The original members of the S. bovis group, which were first recognized as one bacterium, were first isolated from cheese and were placed into the Lancefield group D of streptococci bacteria based on similar morphological characteristics and similarities in preferences for growth mediums. Enterococci strains were also originally classified into the S. bovis group, but were differentiated soon after because of their ability to grow in 6.5% NaCl, hydrolyze arginine, and decarboxylate tyrosine. All members of the SBSEC complex are small-colony, catalase-negative, Gram-positive cocci and can all be detected using the Rapid ID 32 strep systems, making them biochemically challenging to differentiate. [3] However, the original identification and classification of the SBSEC complex were based solely on loosely shared morphological characteristics, and it was clear that new methods for identification should be developed in order to accurately diagnose animals and humans infected with the bacteria.

Modern identification

To differentiate between the eight subspecies, several methods can be used. S. gallolyticus subsp. gallolyticus is mannitol-positive after fermentation, where S. infantarius subsp. infantarius and S. gallolyticus subsp. pasteurianus would be mannitol-negative. S. infantarius subsp. infantarius and S. gallolyticus subsp. pasteurianus test positive for activity in the alpha- and beta-galactosidase enzymes, while S. gallolyticus subsp. gallolyticus would test negative. The beta-glucoronidase enzyme can also be used to differentiate because S. gallolyticus subsp. pasteurianus tests positive and S. gallolyticus subsp. gallolyticus tests negative. Starch degradation is another method for differentiating between the subtypes, because S. infantarius subsp. infantarius typically tests positive for starch degradation while S. gallolyticus subsp. gallolyticus tests negative. For more fast-paced and reliable identification, MALDI-TOF mass spectrometry systems can be used.

Habitats, colonization, and infection associated with the Streptococcus bovis/Streptococcus equinus complex. Numbers refer to sections of the original published review. Streptococcus bovis equinus complex habitats and infection overview.webp
Habitats, colonization, and infection associated with the Streptococcus bovis/Streptococcus equinus complex. Numbers refer to sections of the original published review.

Ecology and natural habitat

Members of the Streptococcus bovis/Streptococcus equinus complex occur in the gastrointestinal tracts of humans and animals, as well as in fermented foods. The historical designation of "Streptococcus bovis" encompassed organisms subsequently assigned to several species and subspecies that have since been distinguished in greater detail. Their individual ecological characteristics are distinct which is an important variable to consider whilst describing their habitats and relationships with the host organisms. [4] [10]

Human GI tract

SBSEC organisms are able to thrive in the intestinal microbiota of completely healthy individuals without causing notable symptoms or disease. Reported carriage frequencies vary with each population examined, specimen type, identification method, and species included, all of which making it very difficult to find substantial data on this microbe. Consequently, historical estimates based on cultures identified as "Streptococcus bovis" are not directly comparable with modern studies targeting individual species or subspecies. [18] Lastly, proven intestinal carriage should be distinguished from invasive infection which will be further elaborated on in the heading of "Human Infection."

In the microbiome of the gut, interactions with other intestinal microorganisms may influence varying effects of colonization. Experimental studies have shown the S. gallolyticus subsp. gallolyticus can produce gallocin, a bacteriocin known to inhibit competing enterococci. [1] In experiments with mice, tumor-associated changes in secondary bile acids enhanced gallocin activity and favored bacterial persistence. [19] These findings describe a potential mechanism of preferential colonization in tumor-bearing hosts rather than the assumption that intestinal carriage causes cancer outright in humans. There is certainly an association to be researched further, but the levels of significance are not yet fully measurable.

Animal reservoirs

The rumen is an important habitat for SBSEC organisms, which participate in carbohydrate fermentation across a wide array of animal groups, namely cows as a common example. Their abundance and metabolic activity are heavily influenced by nutritional availability and feed composition. Sudden increases in fermentable carbohydrates can promote bacterial growth and acid production leading to ruminal acidosis. [20] Historical ruminal samples and isolates described as "Streptococcus bovis" encompass organisms that require revaluation under recent modern clarifications. One of which recently, S. ruminicola was described from the rumen of Korean domestic ruminants, distinct from older texts of "Streptococcus bovis" in the region.

SBSEC organisms have also been recovered from poultry, pigs, household pets, and wildlife. S. gallolyticus subsp. gallolyticus has been identified in Turkey feces and pigeon digestive tracts. Shared sequence types between human and animal isolates, along with associations between human carriage and animal contact, support decent evidence of the transmission between these hosts. However, these observations do not establish the frequency, or holistic direction of zoonotic transmission. [21]

Geographical distinctions

Regional differences in SBSEC ecology include associations with traditional fermented foods showing noticeable differences between Europe, West Africa, East Africa, and East Asia. A recent study of S. infantarius subsp. infantarius established the occurrence of fermented dairy products in East and West Africa. Research has distinguished a major dairy-associated lineage from some human-associated lineages, although ecological groups are not completely separated. [22] These findings indicate the species identification on its own does not dictate a pathological potential in an organism.[ citation needed ]

Conversely, dairy origin also does not indicate safety for human consumption or probiotic use. An experimental investigation of two dairy-derived S. infantarius subsp. infantarius strains evaluated both potentially beneficial characteristics, along with virulence-related conditions. The researchers concluded that both strains showed enough risk to be considered unsafe for human or animal application. [23] However, this conclusion applies only to this specific test of strain rather than establishing all members of the subspecies have identical properties across all organisms. Some medical application may become derived from these strands of the SBSEC in the future, though currently they are wildly associated with clinical diagnostics and disease prediction.[ citation needed ]

The distribution of organisms in clinical collections varies drastically across general study settings. [24] In Hiroshima, Japan, S. gallolyticus subsp. pasteurianus accounted for 209 of 39 bloodstream isolates, whereas subsp. gallolyticus accounted for five. [25] A German investigation of 58 bloodstream isolates identified 29 as subsp. gallolyticus, 12 as subsp. pasteurians, and 17 under the name S. infantarius subsp. coli, now also known as S. lutetiensis. [26] These findings describe very specific clinical collections and do not reflect national intestinal carriage rates. Differences in laboratory identification further complicate comparisons between studies, though all together can provide a rough idea of prevalence across certain countries.[ citation needed ]

Human infection

Organisms historically identified as "Streptococcus bovis" have been implicated in several different human infections all loosely associated with functions of the gastrointestinal tract. In clinical settings, subspecies are not always individually identified in basic testing, as testing can be expensive, time-consuming and the subspecies have similar clinical implications. [27] However, recent advancements in the effectiveness of MALDI-TOF has made subspecies identification more practical and may result in more research on the individual infection routes and disease implications on individual subspecies, most notably, Streptococcus gallolyticus subsp. gallolyticus. [28] [29]

Recent literature tends to use individual subspecies identification when discussing individual cases of bacteremia and infective endocarditis, rather than using the past grouping of SBSEC. [30] [31] Previous clinical implications of S. bovis as a human pathogen implicated as a causative agent of endocarditis, urinary tract infections, and more rarely, sepsis and neonatal meningitis. [32] [33] [34] is more frequently attributed to individual species.

Species and Clinical Associations

Subspecies and their Clinical Associations [35] [36] **
SubspeciesClinical Association
S. gallolyticus subsp. gallolyticus (Sgg)Strong Association with Colorectal Cancer [35] [36]

Association also found between Sgg and [35] [36]

  • Bacteremia
  • Infective endocarditis
  • Biliary tract infections
S. gallolyticus subsp. pasteurianus (Sgp)Common cause of bacteremia. [35] [36]

Also associated with:

  • Adult and neonatal bacterial meningitis [37]
  • Infective endocarditis [36]
  • Biliary tract infections [36]
  • Other malignancies [36]
  • Less common association with colorectal cancer [35]
S. infantarius subsp. coli (Sic)Associated with:
  • Bacteremia [36] [35]
  • Infective endocarditis [36]
  • Biliary tract infections [36]
  • Observed with Pancreatic cancer [35]
  • Rare reported neonatal meningitis [38]
S. infantarius subsp. infantarius (Sii)Associated with:
  • Bacteremia [36] [35]
  • Association with colorectal polyps [36]
  • Observed with colorectal and pancreatic cancer [35]

**It is important to note that not all subspecies are included within this chart, as more recently discovered species have little or weak clinical associations in current research.

Biotype I: S. gallolyticus subsp. gallolyticus (Sgg)

Morphology and cellular structure

Like other microbes within the SBSEC, S. gallolyticus subsp. gallolyticus (Sgg) is a Gram-positive, non-motile, non-spore forming streptococcus. [39] [19] [40] Sgg cell walls are composed of thick peptidoglycan, lipoteichoic acids, and Lancefield group D antigen. These cells are spherical or ovoid-shaped and occur in pairs or short-to-medium chains. [41] The presence of a polysaccharide capsule camouflages them from the innate immune system. [42] [43]

S. gallolyticus subsp. gallolyticus is unique in that it possess three pilus operons that are linked to encoding pili: Pil1, Pil2, and Pil3. [44] [19] [42] While other members of the SBSEC possess the genetic basis for pili, the presence of three in Sgg makes it especially equipped to bind to hosts. [19] [45] Pil1 is exclusive to Sgg and allows it to bind to factor XII in collagen binding proteins, which contributes to the virulence of this subspecies. [46] [43] It also has the ability to form strong biofilms, which protect it from conditions within the host's body. [42] [19] Despite being a Gram-positive bacteria, the phosphate group is found on the reducing end of Sgg, which is a feature most commonly associated with Lipopolysaccharide structures of Gram-negative cell walls. [42]

Sgg houses plasmids that are common in Gram-positive pathogens, along with a variety of other plasmids that suggest lateral transfer in the microbe. [45] The SPAR locus is another unique feature in Sgg that has been directly associated with tumor formation and rapid reproduction. [47] When SPAR has been removed, Sgg loses these features. [47]

Growth and culture characteristics

Streptococcus gallolyticus subsp. gallolyticus shares most of its culture characteristics with other SBSEC species. It is a facultative anaerobe that grows optimally at 35°C-37°C. There is differentiation in the microbe's inability to grow in 4% NaCl that differed from other species in the group. [40] [48] Sgg grows well on nutrient-rich, complex media. In many laboratory protocols, cultures are incubated in an atmosphere enriched with carbon dioxide. In one study, isolates were subcultured on sheep blood agar for 20-24 hours at 35°C in 5% carbon dioxide. [48] Other studies cultured the subspecies on brain-heart infusion agar at 37°C. [48] Colonies on blood agar tend to be small and non-beta-hemolytic, with alpha or gamma hemolysis being reported among SBSEC members. [49]

Metabolism and biochemical characteristics

Streptococcus gallolyticus subsp. gallolyticus has developed distinct metabolic features from other SBSEC species. [44] While other species have evolved to have smaller genomes and have lost some features, Sgg has additional pili genes and unique metabolic features. [44] [46] Sgg is a chemoorganoheterotroph that has the ability to utilize diverse carbohydrates from the environment. [44] [46] This includes carbohydrates unique to plant-life, which is a feature that has allowed Sgg to be especially successful within the gastrointestinal tracts of rumen. [44] [46] Sgg uses 33 different hydrolases, which allows it to effectively break down bonds. [46] The unique metabolic function of Sgg can be attributed to extensive phosphotransferase systems, which allow sugar to be used in metabolism as it is brought into the cell. [46]

Sgg can synthesize all 20 amino acids, making it independent, but it can also synthesize more vitamins than any other species within the Streptococcus genus. [46] This is attributed to lateral gene transfer during interactions with other bacteria in the GI tract of rumen. [46]

Ecology and colonization

Sgg often colonizes in the gastrointestinal (GI) tracts of both animals and humans and presents most commonly in rural or agricultural regions where contact with infected dairy products, red meat, or plant fertilizer may be more common. [50] Observed patients have experienced changes their gut microbiome, which could be caused by competition with Sgg or from the antibiotics used to treat Sgg. [50] Sgg presents similarly among all infected organisms, but specific strains of Sgg may more commonly infect certain species. [50] Certain strains potentially serve as primary pathogens in turkeys. [51]

Pathogenesis

Sgg is thought to be a zoonotic disease by having the ability to transfer between humans and animals, most commonly livestock such as cows or chickens. [50] Sgg can be classified as "opportunistic," and in rare cases, they may be play a role in endocarditis by invasion of the bloodstream and heart valves and adherence to already-weakened endothelial tissue. [51] Sgg is a highly adaptive subspecies, largely due to it's large number of regulatory genes, which are genes that it can conditionally activate in conditions where it is advantageous (7.7%). [46] This high number of regulatory genes is comparable to other opportunistic pathogens, such as Pseudomonas aeruginosa. [46]

Sgg binds to host collagen and fibrinogen through, which contributes to the pathogenicity of the subspecies by allowing it to attach to collagen rich heart valves and to the epithelial cells of the intestinal tract especially well. [52] This can largely be attributed to the pilus operons. [19] [45] [52]

Capsule and biofilm formation are also features that contribute to pathogenicity. [53] Capsule formation allows Sgg to evade immune response and modulate immune responses through degradation enzymes found within capsule genes. [53] [54] Sgg has the ability to form biofilms as well, which creates layering of Sgg microbes, forming a plaque that protects against abrasion. [53] This has been attributed to the microbe's treatment resistance, as penetration of this biofilm can be difficult. [53] In addition, Sgg utilizes quorum-sensing alongside biofilm formation, which allows Sgg to secrete inhibitors based on population density that act against other Streptococcus species, reducing the competition in the environment for the microbe. [55]

The accessory genome of Sgg contains characteristics that contribute to the microbe's ability to colonize within the intestinal tract. [53] The genome contains genes for T7SS, which is a protein secretion system that allows a bacterium to communicate with other microbes and the host. [53] T7SS is associated with the species' ability to colonize the intestinal tract and maintain high populations through inhibiting host immune response and competing bacteria. [56] When T7SS was removed, the microbe lost much of it's ability to populate at high levels and some virulence characteristics, indicating this is an important component of the bacteria's ability to reproduce in the host. [56] In addition, genes that encode for bile-salt resistance and fatty acid metabolism contribute to the cell's viability within the intestinal tract of its host. [53] [57] The accessory genome can vary between strains of Sgg, and not every microbe has the same pathogenic potential. [53]

Disease associations with Streptococcus gallolyticus subsp. gallolyticus

Association with colorectal cancer

Streptococcus gallolyticus subsp. gallolyticus is the species within the SBSEC that is most strongly associated with colorectal cancer. [35] A 2025 study of clinical Sgg isolates found that 55% of the strains found in humans had some association with colorectal cancer. [58]

The same study found that no particular feature in the genome was associated with colorectal cancer, indicating that the relationship between Sgg is complex and not caused by a particular strain or direct pathway. [58] Sgg is known to reproduce more effectively in environments where tumors are present. [59] Sgg is involved in transcriptional reprogramming of genes, which induces tumor growth and development. [60] A bidirectional relationship between colorectal cancer and Sgg has been suggested as Sgg stimulates increased production of collagen in colorectal cancer cells, which in turn improves Sgg's ability to adhere to these cells. [61] Sgg is also able to alter the extracellular matrix through increasing the collagen production of CRC cells, which in turn also promotes tumor growth. [61] Due to the diversity in strains of Sgg and the complex relationship, the exact relationship and directionality is still being researched. [58]

Bacteremia

Bacteremia is a condition associated with most species within the SBSEC. [36] The main portal of entry for human infection of S. bovis bacteremia is the gastrointestinal tract, but in some cases, entry is through the urinary tract, the hepatobiliary tree, or the oropharynx. [62] The ability of the pathogen to survive in the blood of a host has been found to vary widely based on strain of Sgg, along with by unique host characteristics [63] Strain UCN34 of Sgg has been found to be especially effective at surviving and multiplying within human blood [64] . Sgg has also been found to interact with elements of the blood's inflammation and clotting mechanisms, a characteristic that is unique to this subspecies. [64] Bacteremia is strongly linked to infective endocarditis when Sgg is the sole pathogen, with 33% of patients with bacteremia in one study, [35] and 40% in another, [36] due to Sgg also having IE.[ citation needed ]

Infective endocarditis

Streptococcus gallolyticus subsp. gallolyticus is the primary pathogen associated with the majority of SBSEC infective endocarditis cases. [65] A 2023 study found that a bacterial infection of S. gallolyticus made patients 2.57 times more likely to develop infective endocarditis when compared to other Streptococcus bacteria. [66]

The Pil1 gene's affinity for collagen makes Sgg especially effective in attaching to collagen rich regions of the body. [43] When a pre-existing vulnerability of the heart valve, whether through damage to the tissue or an artificial valve being placed, and bacteremia with Sgg are present at the same time, the collagen-binding proteins and pili of Sgg are able to target the exposed ECM and adhere to damaged heart valves. [67]

Antibiotic resistance of Streptococcus gallolyticus subsp. gallolyticus strains

Sgg strains often show antibiotic resistance, and in an analysis of 30 SGG isolates in 2025, 85% were found to carry at least one antibiotic resistance gene. [58] Sgg is especially resistant to tetracycline, due to overuse in agricultural contexts. [58] Macrolides, another antibiotic acting upon bacterial ribosomes, are also an antibiotic that some Sgg strains have developed resistance against. [58] Combined resistance to aminoglycosides and macrolides has also been found in a study, as a result of transposons. [68]

Most Sgg strains isolated from humans are resistant to multiple antibiotics, likely due to C5a peptidase to break down host immunity, T7SS, capsule features, biofilm formation, and bile-salt resistance. [58]

The most common treatment for Sgg infections is the combination of a penicillin and an aminoglycoside. [68] Penicillin-resistance has been limited [69] , one study expresses concern in light of developing resistance against other types of antibiotics and ability to utilize horizontal gene transfer and transposons. [68]

References

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