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Significance and Roles of Proteus Spp. Bacteria in Natural Environments

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Significance and Roles of Proteus Spp. Bacteria in Natural Environments Microb Ecol (2016) 72:741–758 DOI 10.1007/s00248-015-0720-6 MINIREVIEWS Significance and Roles of Proteus spp. Bacteria in Natural Environments Dominika Drzewiecka1 Received: 22 July 2015 /Accepted: 13 December 2015 /Published online: 9 January 2016 # The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Proteus spp. bacteria were first described in 1885 these microorganisms in bioremediation and environmental by Gustav Hauser, who had revealed their feature of intensive protection. swarming growth. Currently, the genus is divided into Proteus mirabilis, Proteus vulgaris, Proteus penneri, Proteus hauseri, Keywords Natural microflora . Symbionts . Pathogens . and three unnamed genomospecies 4, 5, and 6 and consists of Fecal pollution . Bioremediation . PGPR 80 O-antigenic serogroups. The bacteria are known to be hu- man opportunistic pathogens, isolated from urine, wounds, and other clinical sources. It is postulated that intestines are Introduction a reservoir of these proteolytic organisms. Many wild and domestic animals may be hosts of Proteus spp. bacteria, which Proteus Like in Homer’s Poem… are commonly known to play a role of parasites or commen- sals. However, interesting examples of their symbiotic rela- Microorganisms belonging to the genus Proteus were first tionships with higher organisms have also been described. described in 1885 by a German microbiologist Gustav Hauser, Proteus spp. bacteria present in soil or water habitats are often who had revealed their ability to swarm on solid surfaces. The regarded as indicators of fecal pollution, posing a threat of name Proteus came from Homer’s BOdyssey^ and its charac- poisoning when the contaminated water or seafood is con- ter Proteus, who could change his shape and had an ability of sumed. The health risk may also be connected with drug- endless transformation. Hauser described two species of the resistant strains sourcing from intestines. Positive aspects of genus: Proteus vulgaris and Proteus mirabilis [81]. The the bacteria presence in water and soil are connected with swarming ability, connected with a change of short swimmer exceptional features displayed by autochthonic Proteus spp. cells into long, poli-nucleous and hyper-flagellated swarmer strains detected in these environments. These rods acquire cells, is especially visible in the second species. This is a various metabolic abilities allowing their adaptation to differ- possible source of the name of P. mirabilis, which in Latin ent environmental conditions, such as high concentrations of means amazing, marvelous, splendid. Hauser might have con- heavy metals or toxic substances, which may be exploited as sidered P. vulgaris to be more common and ordinary; there- sources of energy and nutrition by the bacteria. The Proteus fore, he gave it the Latin name meaning widespread, usual. spp. abilities to tolerate or utilize polluting compounds as well The ability of swarming growth is used in a simple and effec- as promote plant growth provide a possibility of employing tive Dienes test to differentiate Proteus spp. strains with dis- criminatory power comparable to ribotyping [114]. The phe- nomenon described by Dienes in 1946 consists in forming * Dominika Drzewiecka boundaries between the swarming growth of different strains, [email protected] while isogenic strains merge with each other (Fig. 1). Howev- er, the background of the expression of the territorial compe- 1 Department of General Microbiology, Institute of Microbiology, tition between two swarming non-isogenic strains still remains Biotechnology and Immunology, University of Łódź, unclear [8, 48]. The formation of the boundaries (Dienes lines) 90-237 Łódź, Poland may depend on different profiles of produced proticines 742 D. Drzewiecka of them (idr and tss) encode cytotoxins and a type VI secretion system, respectively [151], while the third one (ids) encodes the Ids proteins responsible for self-identification [21, 49]. However, the mutation in the ids genes does not provoke the killing of parent or mutant strain cells, although the Dienes line is visible between their swarms [48]. The genus Proteus includes Gram-negative, facultative an- aerobic, heterotrophic, and proteolytic rods being human op- portunistic pathogens. The taxonomic classification of these bacteria has changed several times. Lately, the only Proteus species with no clinical significance, Proteus myxofaciens,has been postulated to be moved from the genus Proteus to a new genus Cosenzaea [47]. Among other changes, the exclusion from the genus Proteus of several species that created new genera Providencia and Morganella is worth mentioning. Fig. 1 P. mirabilis strains swarming on the surface of an agar plate: These three closely related genera have formed the tribe isogenic A and B (no line of demarcation is visible) versus unrelated C Proteeae in the family Enterobacteriaceae [81]. Currently, (clear Dienes line of demarcation) the genus Proteus consists of P. mirabilis, P. vulgaris, Proteus penneri, Proteus hauseri, and three genomospecies 4, 5, and (Proteus bacteriocines) and different profiles of strain sensi- 6. P. hauseri as well as the genomospecies were separated tivity [129]. Budding et al. [19] suggested that one of the from P. vulgaris on the grounds of molecular studies and form meeting strains dominated over the other killing it in the P. vulgaris group. The genomospecies 4, 5, and 6 are marked cell–cell contact because round dead cells were observed near only with numbers as there have been no metabolic properties the border in the swarm of the dominated strain. The Dienes indicated to allow their full differentiation [104]. The main reaction is connected with at least three recognized gene clus- biochemical features typical of the genus and distinguishing ters enabling the self-recognition of P. mirabilis bacteria. Two Proteus species are summarized in Table 1. Table 1 The main metabolic characteristics of Proteus spp. Feature P. mirabilis P. penneri P. vulgaris P. hauseri P. genomospecies 4, 5, [103, 104]: B+^positive in 100 % and 6 strains; B−^negative in 100 % strains; in the other cases, the Typical of the genus and distinguishing it from the other Enterobacteriaceae percentage of strains exhibiting Phenylalanine deaminase +(98%) +(99%) + + + positive reaction is given in Lysine decarboxylation − − − − − parentheses Arginine hydrolysis − − − − − Urease production +(98%) + +(86%) + + Glucose fermentation + + + + + Mannose fermentation − − − − − Lactose fermentation − (2 %) − (1 %) − − − Methyl-red +(97%) + +(86%) + + Growth in KCN +(98%) +(99%) +(99%) + +(97%) Tyrosine clearing +(91%) + + + + Typical of the species and allowing their differentiation Ornithine +(99%) − − − − decarboxylation − (2 %) − + + + Indole production +(92%) − (35 %) − (14 %) − +(97%) Lipase production +/− (50 %) − (12 %) + − +(85%) DNase production − +(96%) + + + Maltose fermentation − (15 %) + + + + Sucrose fermentation − − + − − (3 %) Salicin fermentation − − + − − (3 %) Esculin hydrolysis +(65%) − − (29 %) − − Citrate utilization Proteus spp. Bacteria in Natural Environments 743 Bacteria from the genus Proteus can also be differ- Urinary tract infections are most frequently ascending, entiated on the basis of their O-antigen variability, al- often connected with the presence of urinary catheters. though serotyping is not included in the routine diag- It should be noticed that Proteus spp. are the most nostics of these rods. So far, there have been established prevalent bacteria, isolated from bladder and kidney 80 O-antigenic serogroups in the genus, some of them stones (70 % of cases). P. mirabilis is the main cause divided into subgroups [7, 67, 135], and many new O of all Proteus spp. infections accounting for 80–90 % of serotypes are still being discovered (D. Drzewiecka, un- them. published data). The chemical structure of the sugar part It is postulated that human intestines are a reservoir of of the lipopolysaccharide may play an important role in Proteus bacteria, especially those belonging to prevailing the adaptation of Proteus spp. bacteria to environmental P. m irabilis species, and they are members of natural fecal conditions and enhancing their pathogenicity, as some O microflora of several percent of human population [124]. serotypes are more prevalent and more frequently isolat- Lately, Porres-Osante et al. [118] reported the presence of ed from clinical sources than the others (Table 2)[7, Proteus spp. bacteria (one P. mirabilis and one P. vulgaris 35, 37, 72, 111, 133]. strain) in fecal samples from 4 % of healthy Spanish vol- Proteus spp. bacteria have been isolated from different hu- unteers. Zilberstein et al. [160], using cultivation methods man and non-human environments and their presence in to study the microbiota in particular parts of the digestive higher organisms, soil, and water is well documented. How- tract, stated that Proteus spp. bacteria were absent from ever, their specific features and roles played in their natural the mouth and the esophagus of healthy volunteers. How- habitats have not been summarized so far. ever, the bacteria were present in comparatively high mean concentrations in the stomach of 8.1 % of volun- teers (105 colony forming units (CFU)/mL), the duodenum Human Beings and Proteus Bacteria—Commensals (45.5 %, 102), the proximal jejunum (45.5 %, 104), the and Parasites proximal ileum (20 %, 106), the distal ileum (19 %, 103.5), the cecum (12.5 %, 104), the colon (ascending, 33.3 %, Proteus
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