Streptococcal Infections
2.24.1 VIBRIO AND ENVIRONMENT
Vibrios are perhaps the most aquatically-related microorganisms involved in human pathogenesis (Thompson et al., 2004). Beside V. cholerae that mostly lives in fresh water (Perez-Rosas & Hazen, 1989) (however, isolated also from both temperate and tropical marine coastal waters), almost all other human pathogenic Vibrios are halophilic, and consequently isolated from coastal water, marine sediments, seaweeds and sea fauna (Hayatet al., 2006). The main transmission of Vibrioinfections is through the consumption of raw or undercooked shellfish or exposure of wounds to warm seawater (Prapaiwonget al., 2009; Córdovaet al., 2002). The high infective dose ofV. cholerae(range of 108to 109cells) (Sacket al., 2004; Codeco, 2001) requires an amplification process that can occur within the gastro-intestinal system of ill people and further excreted in feces or environmentally in symbiosis with aquatic organisms. Among these organisms, amoebae are the best candidates resembling phagocytes,
2.24.1AnimalsourcesofzoonoticVibriospp.relatedtohumandiseases. Zoonotic(Risk)AnimalGastroenteritisWound InfectionPrimary SepticemiaRef. alginolyticusyesFin-andshellfish+++1 choleraenon-O1yesShellfish,crab,shrimp++++2 choleraeO1yesFish++3 cincinnatiensisNo–++++4 (Vibrio)damselayesFish++5 furnissiiyesEel,shrimps++6 (Vibrio)hollisaeyesFish++++7 fluvialisyesLobster++++8 metschnikoviiyesClam+9 mimicusyesCrayfish++++10 parahaemolyticusyesFish++++11 vulnificusyesEel,fish+++++12 harveyi(=V.carchariae)yesShark++13 on;+Occasional;+Rare T.,Morita,M.,Muramatsu,H.,Monji,A.,Miyagishima,D.,Kanno,T.,Maekawa,M.,2005.AntibioticresistanceinAeromonashydrophilaandVibrio lyticusfromawoundinfection:acasereport.J.Trauma-InjuryInfect.Crit.Care58,196–200. nathan,T.R.,Rathore,G.,Sood,N.,Abidi,R.,Likra,W.S.,2007.Vibriocholeraenon-O1andnon-O139serogroupisolatedfromornamentalfishin IndianVet.J.84,1023–1025. J.G.,2003.Choleraandothertypesofvibriosis:astoryofhumanpandemicsandoystersonthehalfshell.Clin.Infect.Dis.37,272–280. ton,P.R.andBode,R.B.(1986)Vibriocincinnatiensissp.nov.,anewhumanpathogen.JClinMicrobiol23,104–108. M.,Teebken-Fisher,D.,Hose,J.E.,FarmerIII,J.J.,Hickman,F.W.,Fanning,G.R.,1981.Vibriodamsela,amarinebacterium,causesskinulcerson elfishChromispunctipinnis.Science214,1139–1140. aes,V.,Castello,A.,Magalhaes,M.,Gomes,T.T.,1993.LaboratoryevaluationonpathogenicpotentialitiesofVibriofurnissii.Mem.Inst.Oswaldo 88,593–597. strosa,F.,Madeira,R.G.,Bourbeau,P.P.,2007.SeveregastroenteritisandhypovolemicshockcausedbyGrimontia(Vibrio)hollisaeinfection.J.Clin. 45,3462–3463. g,K.C.,Hsu,R.W.W.,2005.Vibriofluvialishemorrhagiccellulitisandcerebritis.Clin.Infect.Dis.40,E75–E77. ,J.D.,1991.RecoveryofVibriometschnikoviifrommarketseafood.J.FoodSafe.12,73–78. ,T.,Sultan,S.Z.,Kaneko,Y.,Yoshimura,T.,Maehara,Y.,Nakao,H.,Tsuchiya,T.,Shinoda,S.,Miyoshi,S.,2009.ModulationofVibriomimicus lysinthroughlimitedproteolysisbyanendogenousmetalloprotease.FEBSJ.276,825–834. ,S.L.,DePaola,A.,Jaykus,L.A.,2007.AnoverviewofVibriovulnificusandVibrioparahaemolyticus.Comp.Rev.FoodSci.FoodSafe.6,120–144. oulos,G.,Stamatakos,M.,Tzurbakis,M.,Batanis,G.,Michou,E.,Iannescu,R.,Safioleas,M.,2008.LowerextremityinfectionsbyVibriovulnificus. irurgia103,201–203. A.T.,Bryan,J.A.,Maher,K.L.,Hester,T.R.,Farmer,J.J.,1989.Vibriocarchariaeinfectionafterasharkbite.Ann.Intern.Med.111,85–86.
Environmental Aspects of Zoonotic Diseases 152
being present in aquatic environments and feeding on different bacteria. Indeed, Abdet al.(2007, 2010) recently showed experimentally an interesting interaction betweenV. choleraeand V. mimicusand the ubiquitous amoebae species,Acanthamoeba castellanii. Both Vibriospecies revealed good growth and multiplication inside the monocellular organisms and also gained protection from antibiotics when encysted. The authors suggested that amoebae may play an important environmental role as host of these pathogens.
In the present chapter, water or foodborne infections will not be described as they were already reviewed in many excellent publications (Tantilloet al., 2004; Mouchtouriet al., 2010; Oliver and Kaper, 1997;
McLaughlin, 1995; Newell et al., 2010); nevertheless, their environmental water aspects associated to zoonoses will be evaluated (Austin, 2010).
Estuarine waters used for aquaculture, fishing and recreational purposes are influenced by a large variety of factors such as climate, tidal flushing, temperature, vertical mixing, precipitation (affecting salinity) and nutrients loading (mainly through sewage discharges). These factors were shown to correlate definitely with Vibriospp. presence and abundance, increasing human and animal infection potential (Hsiehet al., 2008;
Inoueet al., 2008; Sedas, 2007). On the other hand“refractory periods”were reported, when in spite of favorable climatic conditions for“cholera”spread, clinical reported cases dropped significantly, mainly due to lack of susceptible hosts (increased immunity in previously exposed populations to infectious V.
choleraestrains) (Koelle, 2009).
Wind as an additional climatic parameter has been suggested as a possible disseminator ofVibrio cholera (Paz and Broza, 2007). Continental winds were shown to carry aero-plankton (tiny insects such as chironomids or non-biting midges and other small flies) contaminated with cholera bacteria from one body of water to an adjacent one. Earlier, Broza et al. (2001) already showed that chironomids egg masses were infected with V. cholerae and can be an aquatic reservoir of this pathogen. Later, adult non-bitting midges (chironomids) were suspected of possibly carrying V. cholerae and becoming windborne (Brozaet al., 2005). Indeed, this hypothesis is sound enough based on the wide spread of this pathogen globally, especially intra-continentally where bodies of water are secluded.
Many articles emphasized the difficulty inherent in cultivatingV. choleraby conventional techniques, mainly in growing them as colonies on differential culture media. In a recent important report, it was shown thatV. cholerae bacteria present in surface water may exist as conditionally viable environmental cells (CVEC), and partially as dormant cells in an aggregate form (biofilms) (Faruque et al., 2006).
When these aggregates were directly inoculated into rabbit intestines they revealed complete virulence recovery. These authors also indicated two kinds of V. cholerae populations excreted in the stools of infected humans, planktonic and aggregates (clumps), with increased virulence of the latter.
Long et al. (2005) found that marine bacteria could inhibit the colonization of marine particles by V. cholera, through biosynthesis of an antibacterial agent controlled by temperature. At elevated temperature the production of this inhibitory agent diminished, giving preferentiality to V.cholera competitiveness and survival by means of particle colonization and biofilm formation. This biological pattern is compliant with El Niño-Southern Oscilliation (ENSO) and monsoonal events that cause water temperature elevation thereupon enhanced cholera outbreaks.
El Niño/La Niña-Southern Oscillation, or ENSO in brief, is a climate pattern (quasi-periodic) observed across the tropical Pacific Ocean (western part), approximately at an average of 5 years intervals (between 2 to 7 years). The main characteristics are variations in ocean water surface temperature (warming or cooling known asEl NiñoandLa Niña, respectively) and air surface pressure in the tropical western Pacific - the Southern Oscillation. In the western Pacific, the two variations are coupled: the warm oceanic phase, El Niño, accompanies high air surface pressure, while the cold phase, La Niña, accompanies low air surface pressure (Figure 2.24.1). It is now clear that this climatic phenomenon has a global impact
Vibrioses 153
causing in other continents a variety of disastrous events (Figure 2.24.2). The oscillation mechanism remains still unclear, but its results are seen in biosphere behavior including cholera outbreaks.
Similar results forV. choleraeO1prevalence were reported in Mexico at different locations (after El Niño and La Nina) (Lizárraga-Partidaet al., 2009). These authors concluded thatV. cholera O1 derives from marine and estuarine origin and not from sewage contamination, linking copepod abundance with climatic conditions. In other locations such as southeastern Africa (a 35 years survey) (Paz, 2009) and South Korea (Heon and Yeon, 2010), the same trend was observed after an increase in sea surface temperature.
Figure 2.24.1. El Niño-Southern Oscillation (ENSO) Phenomenon. (2002) InUNEP/GRID-Arendal Maps and Graphics Library. Retrieved 14:53, January 2, 2011 from http://maps.grida.no/go/graphic/ el-ni-o-southern-oscillation-enso-phenomenon, credit to Delphine Digout, UNEP/GRID-Arendal (Climate Prediction Center (CPC), National Centers for Environmental Prediction (NCEP); National Oceanic and Atmospheric Administration (NOAA)
Environmental Aspects of Zoonotic Diseases 154
V. vulnificusclinical cases in fish industry workers linked to high summer temperatures. In colder temperate geographical areas such as Denmark,V. vulnificuswas also reported to infect people during a particularly warm summer (Bruunet al., 1996).
Figure 2.24.3 summarizes the global spread of cholera from 1950 to 2004. For 20 years it spread from the most endemic area (India) towards China in the north, Iran in the west and Indonesia in the east.
After an additional 20 years the disease agent spread globally to North and South America, Europe, Russia and even Australia.
Mezrioui and Oufdou (1996) reported on non-O1 Vibrio cholera survival in a simple domestic wastewater treatment (stabilization ponds) versus the decline of indicator bacteria (fecal coliforms).
Figure 2.24.2. El Niño phenomenon impact on climate of South and Central America (2005). InUNEP/ GRID-Arendal Maps and Graphics Library. Retrieved 14:55, January 2, 2011 from http://maps.grida.no/go/ graphic/climate_impacts_of_el_ni_o_phenomenon_in_latin_america_and_the_caribbean, credit to UNEP/GRID-Arendal (IPCC 2001, FAO 2002, UNEP 2003)
Vibrioses 155
Seasonal distribution was reversed with increased survival of non-O1Vibrio cholerawith high densities in hot periods and low densities in cold periods.
Aquatic plants, seaweeds, and free floating phyto- and zooplankton can harbor vibrios in viable but nonculturable (VBNC), sporelike forms, as demonstrated by fluorescent antibody and polymerase chain reaction techniques (Islam et al., 1989; Huq et al., 1990). There is no reason to suspect that affinity for algae and weeds differs among various marine vibrios (Islam et al., 1990*; Islam et al., 1990).
The growth of marine and freshwater photosynthesizers is prompted by nitrogen-rich wastewater, fertilizers, acid rain, and runoff soil (eutrophication) that may enhance also the growth of pathogenic Vibrios.
In contrast to tropical or subtropical seas, along the Swedish coastline (Skagerrak Sea) where the average temperature is∼5°C, Vibrios population was studied and surprisingly found to be widespread (Eileret al., 2006). Total Vibrios spp. abundance was found to range from 103to 104cells/L with increasing numbers in more saline waters.V. anguillarum and V. aestuarianusgenotypes were present in brackish waters. In addition, 50% of the samples were positive for V. choleraandV. mimicus(.103cells/L) in very cold Figure 2.24.3. Global cholera spread from 1950 to 2004. (With permission from: The spread of cholera 1950-2004. (2009). InUNEP/GRID-Arendal Maps and Graphics Library. Retrieved 20:56, January 19, 2011 from http://maps.grida.no/go/graphic/the-spread-of-cholera-1950-2004, credit to UNEP/GRID-Arendal (Working group II and III, Synthesis Report, IPCC, 2007)
Environmental Aspects of Zoonotic Diseases 156
coastal line. These findings may explain the reports of wounds infected byV. cholerain Swedish swimmers (Andersson and Ekdahl, 2006; Rehnstam-Holm & Collin, 2009).
Using an experimental approach, Wiklundet al.(2009) looked for structural changes in the pelagic food web under temperature alteration by 5°C in a Baltic Sea mesocosm (a brackish sea water with a salinity of
∼7‰near the coastal line and 10–15‰in the open, compared to 35‰found in oceans) using the amphipod Monoporeia affinisas a key benthic species. They found a structural shift in the pelagic food web from one based on algae to one based on bacteria, which decreased amphipod productivity and the efficiency of the pelagic-benthic food web (FWE). As growth of amphipods and FWE were not directly affected by the temperature raise, the authors concluded that the main ecological impact occurred through indirect structural changes in the pelagic food web and consequently on the benthic productivity. As Vibrio species also belong to the benthic food web it is very much possible that temperature rise will increase human health risk in these environments.
2.24.2 REFERENCES
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Abd, H., Valeru, S.P., Sami, S.M. Saeed, A., Raychaudhuri, S. & Sandström, G. (2010) Interaction betweenVibrio mimicusandAcanthamoeba castellanii. Environ Microbiol Rep2, 166–171.e.mi4_ 166
Andersson, Y. & Ekdahl, K. (2006) Wound infections due to Vibrio cholerae in Sweden after swimming in the Baltic Sea, summer 2006.Euro Surveill.11, E060803.2.
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Broza, M. & Halpern, M. (2001) Pathogen reservoirs: chironomid egg masses andVibrio cholerae. Nature412, 40.
Broza, M., Gancz, H., Halpern, M., Kashi, Y. (2005) Adult non-biting midges: possible windborne carriers ofVibrio cholerae. Environ Microbiol7, 576–585.
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Campanelli, A., Sanchez-Politta, S. & Saurat, J.H. (2008) Cutaneous ulceration after an octopus bite: infection due to Vibrio alginolyticus, an emerging pathogen.Ann Dermatol Venereol135, 225–227.
Codeco, C.T. (2001) Endemic and epidemic dynamics of cholera: the role of the aquatic reservoir.BMC Infect Dis.
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Córdova, J.L., Astorga, J., Silva, W. & Riquelme, C. (2002) Characterization by PCR ofVibrio parahaemolyticus isolates collected during the 1997-1998 Chilean outbreak.Biol. Res.35, 433–440.
Eiler, A., Johansson, M. & Bertilsson, S. (2006) Environmental influences on Vibrio populations in northern temperate and boreal coastal waters (Baltic and Skagerrak Seas).Appl. Environ. Microbiol.72, 6004–6011.
Faruque, S.M., Biswas, K., Udden, S.M.N., Ahmad, Q.S., Sack, D.A., Nair, G.B. & Mekalanos, J.J. (2006) Transmissibility of cholera: In vivo-formed biofilms and their relationship to infectivity and persistence in the environment.Proc. Natl. Acad. Sci. U.S.A.103, 6350–6355.
Hayat, M.Z., Afework, K., Alizadeh, M., Masayuki, Y., Bhuiyan, N.A., Balakrish, N.G. & Fusao, O. (2006) Isolation and molecular characterization of toxigenicVibrio parahaemolyticusfrom the Kii Channel, Japan.Microbiol. Res.
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Heon, K.S. & Yeon, J.J. (2010) Correlations between climate change-related infectious diseases and meteorological factors in Korea.J Prev Med Public Health43, 436–444.
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Huq, A., Colwell, R.R., Rahman, R.et al.(1990) Detection of Vibrio cholerae O1 in the aquatic environment by fluorescent-monoclonal antibody and culture methods.Appl Environ Microbiol.56, 2370–2373.
Inoue, Y., Ono, T., Matsui, T., Miyasaka, J., Kinoshita, Y. & Ihn, H. (2008) Epidemiological survey ofVibrio vulnificus infection in Japan between 1999 and 2003.J. Dermatol.35, 129–139.
Islam, M.S., Drasar, B.S. & Bradley, D.J. (1989) Attachment of toxigenic Vibrio cholerae O1 to various fresh water plants and survival with a filamentous green algae,Rhizoclonium fontanum. J Trop Med Hyg.92, 396–401.
Islam, M.S., Drasar, B.S. & Bradley, D.J. (1990)* Longterm persistence of toxigenic Vibrio cholera O1 in the mucilaginous sheath of a blue-green algae,Anabaena variablis. J Trop Med Hyg.93, 133–139.
Islam, M.S., Drasar, D.S. & Bradley, D.J. (1990) Survival of toxigenicVibrio choleraeO1 on a duckcweed,Lemna minor, in artificial aquatic ecosystems.Trans R Soc Trop Med Hyg.84, 422–424.
Koelle, K. (2009) The impact of climate on the disease dynamics of cholera.Clin Microbiol Infect15 (Suppl. 1), 29–31.
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(2009) Association of Vibrio cholerae with plankton in coastal areas of Mexico. Environ. Microbiol. 11, 201–208.
Long, R.A., Rowley, D.C., Zamora, E., Liu, J., Bartlett, D.H. & Farooq Azam, F. (2005) Antagonistic Interactions among Marine Bacteria Impede the Proliferation ofVibrio cholera. Appl. Environ. Microbiol.71, 8531–8536.
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Mezrioui, N. & Oufdou, Kh. (1996) Abundance and antibiotic resistance of non-O1Vibrio choleraestrains in domestic wastewater before and after treatment in stabilization ponds in an arid region (Marrakesh, Morocco).FEMS Microbiol. Ecol.21, 277–284.
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Newell, D.G., Koopmans, M., Verhoef, L., Duizer, E., Aidara-Kane, A. et al.(2010) Food-borne diseases - The challenges of 20 years ago still persist while new ones continue to emerge.Int. J. Food Microbiol.139, S3–S15.
Oberbeckmann, S., Wichels, A., Maier, T., Kostrzewa, M., Raffelberg. S. & Gerdts, G. (2011) Apolyphasic approach for the diferentiation of environmental Vibrio isolates from temperate waters.FEMS Microbiol. Ecol.75, 145–162.
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Montville, T.J., pp. 228–264. ASM Press, Washington, D.C.
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Chapter 2.25 Yersinioses
[YERSINIA ENTEROCOLITICAANDYERSINIA PSEUDOTUBERCULOSIS] Both Y. enterocoliticaandY. pseudotuberculosis belong to the family of Enterobacteriaceae and genus Yersinia like their previously described relative:Y. pestis. These species are gram-negative coccobacilli, facultative anaerobes that primarily cause zoonotic diseases. Among the ∼50 serovars (serogroups) of Y. enterocolitica, only serogroups O:3, O:9 (Europe), O:8 (USA), O:5 and O:27 (Japan and Canada) were identified as human pathogens. Y. pseudotuberculosis has 14 serovars of which O:1 constitutes 60–70% while O:2 and O:3 constitutes 10–20% (in Europe), O:4 and O:6 (mainly in Japan). The main reservoirs of these bacteria are rodents and birds with cross-transmission to humans, farm animals, pets, laboratory and wild animals, animal food and water (Mollaret, 1983). The diseases caused by these two species are enteritis/enterocolitis with symptoms such as: febrile diarrhea, pseudo-appendicitis, septicemia, erythema nodosum, arthritis, mesenterial lymphadenitis, etc.
2.25.1 Y. ENTEROCOLITICA, Y. PSEUDOTUBERCULOSIS AND ENVIRONMENT (FIGURE 2.25.1)
Both pathogens, Y. enterocolitica and Y. pseudotuberculosis, are well documented zoonotic foodborne pathogens (otherwise called“saprozoonoses”) (Krausset al., 2003), transmitted through direct contact or via water and food obtained from contaminated animals (farm animals: pigs, cattle, etc.) (Fredriksson-Ahomaa et al., 2007). In this section, the foodborne aspect will not be discussed since it was reviewed elsewhere in details (Matargas and Drosinos, 2009; Dube, 2009).
Litvin et al. (1991) showed that plants such as cabbage, lettuce, pea and oat, challenged with Y. enterocoliticaandY. pseudotuberculosisoriginating from soil and water revealed internal penetration of these plants (roots, seeds and leaves) and survival for up to 30 days.
A similar plant connection was reported in Finland, where an outbreak ofY. pseudotuberculosisoccurred among schoolchildren who fed on infected carrots (Jalavaet al., 2006). It is not clear if the carrots were
for this bacterium. In Finland also, Nuorti et al. (2004) reported on a nation-wide infection with Y. pseudotuberculosis O:3 originating from iceberg lettuce. Interestingly, the authors mentioned an ecologically distinct feature of a large population (.10,000 animals) of nonnative roe deer (Capreolus capreolus)introduced in the 1960s as well as large quantities of roe deer feces found all over the lettuce fields and around every one of the irrigation water sources.
It is very feasible that soil is the main link between pathogens and cultivable plants. Barreet al.(1977) isolated differentY. pseudotuberculosisserotypes among which serotype I (an already demonstrated human pathogen) from soil samples around Paris (France) while Nastasiet al.(1986) isolatedY. enterocoliticafrom soil and dog feces. These reports suggest a clear potential health risk from soils as a reservoir for these pathogens. Also in relation to soil, Y. pseudotuberculosiswas studied for its persistence in sterile soils (as an abiotic environment) and in natural soil (as biotic/abiotic multifaceted environment) (Litvinet al., 1990). In sterile soil, Y. pseudotuberculosiswas resistant to a wide range of temperatures (0 to 30°C), humidities (15 to 50%) and pHs (5.9 to 9.0). Under these conditions, the growth rate was only slightly affected but not the general nature of the population dynamic of this bacterium. A more marked impact was observed in natural soil containing other bacterial species such asAcinetobacter andPseudomonas that can alter Y. pseudotuberculosis biotic persistence. According to the authors’ results, another Figure 2.25.1. Y. enterocoliticaandpseudotuberculosisspp. presence and interaction with
environmental parameters
Yersinioses 161
important biotic factor is the endosymbiotic relationship between Y. pseudotuberculosisand free-living infusorianTetrahymena pyriformis, shown to sustain this pathogen population in soil and water.
The saprophitic characteristics of Y. pseudotuberculosis were shown in soil samples from the surroundings of Nero lake (Rostov district, Russia), which is a natural source of this pathogen (Maksimenkova & Karpachevskii 1985). Soil in this area has a high content of organics, cations exchange capacity (CEC) and moisture, all favoring the growth and survival of thess organisms for prolonged periods. Soil survival of Y. enterocolitica was studied in natural soil, river water and well water (Tashiroet al., 1991). AmongY. enterocoliticaserotypes O:3, O:4, O:5A, O:5B, O:6, O:6, O:30, O:9 and O:13 seroptypes O3, O:5B and O:9 strains survived longer at 4°C than at 20°C in these soil and river water environments.
Aksenovet al.(1995) and Troitskaiaet al.(1996) found higher numbers ofY. pseudotuberculosisin environmental soil samples from natural foci using the specific molecular method (PCR) than using the classical culture method. This detection disparity was attributed to a viable but non-culturable (VNBC) form of Y. pseudotuberculosis. VNBC forms of Y. pseudotuberculosis were also observed in soil in association with blue-green algae, Anabaena variabilis, closely related to seasonal changes such as temperature (Solokhinaet al., 2001). Exometabolites of these algae accelerated the formation of“resting cells” of Y. pseudotuberculosis at 22°C. When VNBC forms were passed through infusoria ciliated protozoa, partial reversion to vegetative form (cells capable of growing on solid culture medium) was observed. The transfer from vegetative to VNBC form in relation to algal soil presence is not clear, but it can be speculated that some“partial antibiotic activity”may be attributed to algal exometabolites that do not eradicate bacterial cells completely but act as a biostatic factor altering their growth capability.
Indeed, lower enzymatic activity, agglutinability, cytopathogenicity and plasmid p45 loss were observed in revertant bacterial cells.
A potential connection to soil types and algal content was also described by Sidorenko and Buzoleva (2007) who compared two seashore soil types (maritime meadow and tidal marsh) for their growth support of two pathogens:L. monocytogenesandY. pseudotuberculosis. Both soil types were supportive for growth and survival, with maritime meadow being superior.
In Germany, soil originating from deciduous forest was found to harborY. enterocoliticain contrast to grassland soil that was found to be negative (Botzler, 1987). In northwest California,Y. enterocoliticawas isolated from soils inhabited by infected wapiti (an elk species,Cervus elaphus roosevelti, L.). Prevalence of Y. enterocoliticain soil from forest habitat was significantly higher than that from prairie habitat especially following a previous excessive rainfall of 17 mm (Botzler, 1979). From these reports it is clear that forest
In Germany, soil originating from deciduous forest was found to harborY. enterocoliticain contrast to grassland soil that was found to be negative (Botzler, 1987). In northwest California,Y. enterocoliticawas isolated from soils inhabited by infected wapiti (an elk species,Cervus elaphus roosevelti, L.). Prevalence of Y. enterocoliticain soil from forest habitat was significantly higher than that from prairie habitat especially following a previous excessive rainfall of 17 mm (Botzler, 1979). From these reports it is clear that forest