Significance of interspecies and intraspecies interactions of microorganisms as a sub-organism level in the hierarchy of the epidemic process
Anatoly A. Yakovlev , Alexey V. Rakov , Ekaterina S. Pozdeeva
Epidemiology and Infectious Diseases ›› 2020, Vol. 25 ›› Issue (3) : 118 -130.
Significance of interspecies and intraspecies interactions of microorganisms as a sub-organism level in the hierarchy of the epidemic process
Currently, the epidemic process is considered a complex multilevel system, which involves the suborganismic (i.e., tissue, cellular, and molecular), organismic, and socio-ecosystem (population). In the human population, many pathogenic microorganisms circulate and may cause disease in humans simultaneously. As a rule, they exist in an associated state – a universal phenomenon for the vast majority of representatives of the microworld. However, possible interrelationships between them and their reflection in the epidemic development process and its `manifestations, as a rule, has not been taken into account. In this study, based on an analysis of publications on the results of our own research by the authors and world literature, at the sub-organism level of the epidemic process there is an active inter- and intraspecies interaction among representatives of different types of microorganisms, realized through integration-competitive mechanisms. This interaction is reflected both at the organism and population levels of the epidemic process. Therefore, when conducting epidemiological studies, an integrative approach is needed to take into account processes happening at a suborganism level. Understanding that microorganisms actively interact with each other will significantly increase our ability to develop new approaches to protect organisms from infections, as well as adequately predict the occurrence and development of an epidemic.
microorganisms / interaction / coinfection / epidemic process / integrative approach
| [1] |
Fernandez L, Mercader JM, Planas-Fèlix M, Torrents D. Adaptation to environmental factors shapes the organization of regulatory regions in microbial communities. BMC Genomics. 2014;15(1):877. doi: 10.1186/1471-2164-15-877 |
| [2] |
Fernandez L., Mercader J.M., Planas-Fèlix M., Torrents D. Adaptation to environmental factors shapes the organization of regulatory regions in microbial communities // BMC Genomics. 2014. Vol. 15, N 1. P. 877. doi: 10.1186/1471-2164-15-877 |
| [3] |
Comolli LR. Intra- and inter-species interactions in microbial communities. Front Microbiol. 2014;(5):629. doi: 10.3389/fmicb.2014.00629 |
| [4] |
Comolli L.R. Intra- and inter-species interactions in microbial communities // Front Microbiol. 2014. N 5. Р. 629. doi: 10.3389/fmicb.2014.00629 |
| [5] |
Almand EA, Moore MD, Jaykus LA. Virus-bacteria interactions: an emerging topic in human infection. Viruses. 2017;9(3):58. doi: 10.3390/v9030058 |
| [6] |
Almand E.A., Moore M.D., Jaykus L.A. Virus-bacteria interactions: an emerging topic in human infection // Viruses. 2017. Vol. 9, N 3. P. 58. doi: 10.3390/v9030058 |
| [7] |
Giaouris E, Heir E, Desvaux M, et al. Intra- and inter-species interactions within biofilms of important foodborne bacterial pathogens. Front Microbiol. 2015;(6):841. doi: 10.3389/fmicb.2015.00841 |
| [8] |
Giaouris E., Heir E., Desvaux M., et al. Intra- and inter-species interactions within biofilms of important foodborne bacterial pathogens // Front Microbiol. 2015. N 6. Р. 841. doi: 10.3389/fmicb.2015.00841 |
| [9] |
Miller GG. Biological significance of microbial associations [Biologicheskoe znachenie assotsiatsii mikroorganizmov]. Annals of the Russian Academy of medical sciences. 2000;(1):45–51. (In Russ). |
| [10] |
Миллер Г.Г. Биологическое значение ассоциаций микроорганизмов // Вестник РАМН. 2000. № 1. С. 45–51. |
| [11] |
Selivanov AA. Ecology of human adenoviruses [Ekologiya adenovirusov cheloveka]. Annals of the Russian Academy of medical sciences. 1983;(5):40−44. (In Russ). |
| [12] |
Селиванов А.А. Экология аденовирусов человека // Вестник Академии медицинских наук СССР. 1983. № 5. С. 40–44. |
| [13] |
Belov AB. Correlation of infection introduction and internal reservoirs of pathogens in the epidemic process. Proceedings of the nauchno-prakt. konferentsiya «Teoreticheskie i prakticheskie aspekty sovremennoi ehpidemiologii»; January 28, 2009. Moscow, 2009. P. 32–44. (In Russ). |
| [14] |
Белов А.Б. Соотношение заноса инфекций и внутренних резервуаров возбудителей в эпидемическом процессе // Материалы научно-практ. конференции «Теоретические и практические аспекты современной эпидемиологии»; Январь 28, 2009. Москва, 2009. С. 32–44. |
| [15] |
Nadaraya GP. The problem of simultaneous spread of various infections (integration epidemiology). Tbilisi; 1980. (In Russ). |
| [16] |
Надарая Г.П. Проблема одновременного распространения различных инфекций (интеграционная эпидемиология). Тбилиси, 1980. |
| [17] |
Andreev IA. Human and bacterial world: problems of interaction [Chelovek i bakterial’nyi mir: problemy vzaimodeistviya]. Vestnik Rossijskoj akademii nauk. 2009;79(1):41−49. (In Russ). |
| [18] |
Андреев И.А. Человек и бактериальный мир: проблемы взаимодействия // Вестник РАН. 2009. Т. 79, № 1. С. 41–49. |
| [19] |
Larin FI, Zhukova LI, Lebedev VV, Rafeenko GK. Interference interaction of viruses in the regulation of an epidemic process. Epidemiology and infectious diseases. 2012;(1):25−29. (In Russ). |
| [20] |
Ларин Ф.И., Жукова Л.И., Лебедев В.В., Рафеенко Г.К. Интерферирующее взаимодействие вирусов в регуляции эпидемического процесса // Эпидемиология и инфекционные болезни. 2012. № 1. C. 25–29. |
| [21] |
Pozdeeva ES, Yakovlev AA. Integratsionnyi metod v epidemiologicheskoi diagnostike gepatitov B i C na modeli Primorskogo kraya. Saarbrucken: Lambert; 2012. (In Russ). |
| [22] |
Поздеева Е.С., Яковлев А.А. Интеграционный метод в эпидемиологической диагностике гепатитов В и С на модели Приморского края. Saarbrucken : Lambert, 2012. |
| [23] |
Chekunina SN, Yakovlev AA, Kolpakov SL. Epidemiological assessment of the integrative and competitive relations between hepatitis A and shigellosis impact on the epidemic process of the infection evolution. Pacific Medical Journal. 2015;(3):35–38. (In Russ). |
| [24] |
Чекунина С.Н., Яковлев А.А., Колпаков С.Л. Эпидемиологическая оценка влияния интеграционно-конкурентных взаимоотношений между гепатитом А и шигеллезами на развитие эпидемического процесса указанных инфекций // Тихоокеанский медицинский журнал. 2015. № 3. С. 35–38. |
| [25] |
Yakovlev AA, Kolpakov SL. Streptococcal infection in seafarers (marine epidemiology). Vladivostok: Medicina DV; 2013. (In Russ). |
| [26] |
Яковлев А.А., Колпаков С.Л. Стрептококковая инфекция у моряков (морская эпидемиология). Владивосток : Медицина ДВ, 2013. |
| [27] |
Yakovlev AA, Lapteva NI. Integration epidemiology of infections with a hemocontact transmission mechanism (HIV, hepatitis B and C) on the model of the Republic of Sakha (Yakutia). Vladivostok: Medicina DV; 2016. (In Russ). |
| [28] |
Яковлев А.А., Лаптева Н.И. Интеграционная эпидемиология инфекций с гемоконтактным механизмом передачи (ВИЧ, гепатиты В и С) на модели Республики Саха (Якутия). Владивосток : Медицина ДВ, 2016. |
| [29] |
Yakovlev AA, Burnasheva LS, Zhdanova SN. Integration epidemiology of tuberculosis and HIV infection (based on the model of the Republic of Sakha (Yakutia). Vladivostok: Medicina DV; 2017. (In Russ). |
| [30] |
Яковлев А.А., Бурнашева Л.С., Жданова С.Н. Интеграционная эпидемиология туберкулеза и ВИЧ-инфекции (на модели республики Саха (Якутия). Владивосток : Медицина ДВ; 2017. |
| [31] |
Cherkassky BL. System approach in epidemiology. Moscow: Meditsina; 1988. (In Russ). |
| [32] |
Черкасский Б.Л. Системный подход в эпидемиологии. Москва : Медицина, 1988. |
| [33] |
Yakovlev AA, Pozdeyeva YS. The need for systems approach to studying the concomitant forms of viral hepatitides. Epidemiology and Infectious Diseases. 2010;15(4):54–57. (In Russ). doi: https://doi.org/10.17816/EID40509 |
| [34] |
Яковлев А.А., Поздеева Е.С. О необходимости системного подхода к изучению сочетанных форм вирусных гепатитов // Эпидемиология и инфекционные болезни. 2010. Т. 15, № 4. С. 54–56. doi: https://doi.org/10.17816/EID40509 |
| [35] |
Yakovlev AA. The concept of integration-competitive development of epidemic process. Pacific Medical Journal. 2006;(3):10–14. (In Russ). |
| [36] |
Яковлев А.А. Концепция интеграционно-конкурентного развития эпидемического процесса // Тихоокеанский медицинский журнал. 2006. № 3. С. 10–14. |
| [37] |
Yakovlev AА, Pozdeeva ES. Possible mechanisms of self-regulation of parasitic systems in the biogeocenosis. Annals of the Russian Academy of Medical Sciences. 2018;73(3):184–194. (In Russ). doi: 10.15690/vramn880 |
| [38] |
Яковлев А.А., Поздеева Е.С. О возможных механизмах саморегуляции паразитарных систем в биогеоценозе // Вестник РАМН. 2018. T. 73, № 3. С. 184–194. doi: 10.15690/vramn880 |
| [39] |
Schmalhausen II. Cybernetic questions of biology. Novosibirsk: Nauka; 1968. (In Russ). |
| [40] |
Шмальгаузен И.И. Кибернетические вопросы биологии. Новосибирск : Наука, 1968. |
| [41] |
Gromashevsky LV. General epidemiology. Moscow: Meditsina; 1965. (In Russ). |
| [42] |
Громашевский Л.В. Общая эпидемиология. Москва : Медицина, 1965. |
| [43] |
Belyakov VD, Yafaev RH. Epidemiology. Moscow: Meditsina; 1989. (In Russ). |
| [44] |
Беляков В.Д., Яфаев Р.Х. Эпидемиология. Москва : Медицина, 1989. |
| [45] |
Litvin VYu, Ginzburg AL. Integrative processes in modern epidemiology. Journal of Microbiology Epidemiology Immunobiology. 2002;(4):63–72. (In Russ). |
| [46] |
Литвин В.Ю., Гинзбург А.Л. Интегративные процессы в современной эпидемиологии // Журнал микробиологии эпидемиологии и иммунобиологии. 2002. № 4. С. 63–72. |
| [47] |
Baroyan OV, Porter DR. The Problem of mixed infections. In: Baroyan OV, Porter DR. International and national aspects of modern epidemiology and microbiology. Moscow: Meditsina; 1975. (In Russ). |
| [48] |
Бароян О.В., Портер Д.Р. Проблема смешанных инфекций // Бароян О.В., Портер Д.Р. Международные и национальные аспекты современной эпидемиологии и микробиологии. Москва : Медицина, 1975. |
| [49] |
Belaya OB, Belaya YuB. The Problem of mixed infections and their diagnostics. In: Belaya OB, Belaya YuB. Mixed infections. Moscow; 1986. (In Russ). |
| [50] |
Белая О.Б., Белая Ю.Б. Проблема смешанных инфекций и их диагностика // Белая О.Б., Белая Ю.Б. Смешанные инфекции. Москва, 1986. |
| [51] |
Nechaev VV, Ivanov AK, Panteleev AM. Socially significant infections. Part II. Saint Petersburg: Beresta; 2011. (In Russ). |
| [52] |
Нечаев В.В., Иванов А.К., Пантелеев А.М. Социально-значимые инфекции. Монография в 2-х частях. Ч. II. Санкт-Петербург : Береста, 2011. |
| [53] |
Savilov ED, Kolesnikov SI, Briko NI. The comorbidity in epidemiology – new trend in public health research. Journal of Microbiology Epidemiology Immunobiology. 2016;(4):66–75. (In Russ). doi: 10.36233/0372-9311-2016-4-66-75 |
| [54] |
Савилов Е.Д., Колесников С.И., Брико Н.И. Коморбидность в эпидемиологии ― новый тренд в исследованиях общественного здоровья // Журнал микробиологии эпидемиологии и иммунобиологии. 2016. № 4. C. 66–75. doi: 10.36233/0372-9311-2016-4-66-75 |
| [55] |
Shkarin VV, Blagonravova AS. Epidemiological features of combined infections. Nizhny Novgorod; 2017. (In Russ). |
| [56] |
Шкарин В.В., Благонравова А.С. Эпидемиологические особенности сочетанных инфекций. Нижний Новгород, 2017. |
| [57] |
Buharin OV. Symbiotic interactions of microorganisms during infection. Journal of Microbiology Epidemiology Immunobiology. 2013;(1):93–97. (In Russ). |
| [58] |
Бухарин О.В. Симбиотические взаимоотношения микроорганизмов при инфекции // Журнал микробиологии эпидемиологии и иммунобиологии. 2013. № 1. С. 93–97. |
| [59] |
Pan’kov AS. Peculiarities of influenza bacterial interactions. Izvestia Orenburg state agrarian university. 2011;(2):278–281. (In Russ). |
| [60] |
Паньков А.С. Особенности межбактериальных взаимодействий при гриппе // Известия Оренбургского государственного аграрного университета. 2011. № 2. С. 278–281. |
| [61] |
Bukharin OV, Lobakova ES, Nemtseva NV, Cherkasov SV. Associative symbiosis. Yekaterinburg: Ural Branch of the Russian Academy of Sciences; 2007. (In Russ). |
| [62] |
Бухарин О.В., Лобакова Е.С., Немцева Н.В., Черкасов С.В. Ассоциативный симбиоз. Екатеринбург : УрО РАН, 2007. |
| [63] |
Bel’skij VV, Shatalova EV. The reciprocal effect of the causative agents in a mixed infection in burn injury. Journal of Microbiology Epidemiology Immunobiology. 1999;(4):3–7 (In Russ). |
| [64] |
Бельский В.В., Шаталова Е.В. Взаимное влияние возбудителей при смешанной инфекции ожоговой травмы // Журнал микробиологии эпидемиологии и иммунобиологии. 1999. № 4. С. 3–7. |
| [65] |
Gincburg AL, Il’ina TO, Romanova JuM. “QUORUM SENSING” or social behavior of bacteria. Journal of Microbiology Epidemiology Immunobiology. 2003;(5):86–93. (In Russ). |
| [66] |
Гинцбург А.Л., Ильина Т.О., Романова Ю.М. «QUORUM SENSING» или социальное поведение бактерий // Журнал микробиологии эпидемиологии и иммунобиологии. 2003. № 5. С. 86–93. |
| [67] |
Nikolaev YuA. Distant information interactions in bacteria [Distantnye informatsionnye vzaimodeistviya u bakterii]. Vestnik Rossijskoj akademii nauk. 2000;(5):597–605. (In Russ). |
| [68] |
Николаев Ю.А. Дистантные информационные взаимодействия у бактерий // Вестник РАН. 2000. № 5. С. 597–605. |
| [69] |
Smillie CS, Smith MB, Friedman J, et al. Ecology drives a global network of gene exchange connecting the human microbiome. Nature. 2011;480(7376):241–244. doi: 10.1038/nature10571 |
| [70] |
Smillie C.S., Smith M.B., Friedman J., et al. Ecology drives a global network of gene exchange connecting the human microbiome. Nature. 2011. Vol. 480, N 7376. Р. 241–244. doi: 10.1038/nature10571 |
| [71] |
Romanova YuM, Ilina TS, Ginzburg AL. Mobile genetic elements and their role in the evolution of pathogenic bacteria [Mobil’nye geneticheskie ehlementy i ikh rol’ v ehvolyutsii patogennykh bakterii]. Annals of the Russian Academy of medical sciences. 2001;(11):15–20. (In Russ). |
| [72] |
Романова Ю.М., Ильина Т.С., Гинцбург А.Л. Мобильные генетические элементы и их роль в эволюции патогенных бактерий // Вестник РАМН. 2001. № 11. С. 15–20. |
| [73] |
Christensen BB, Sternberg C, Andersen JB, et al. Establishment of new genetic traits in a microbial biofilm community. Appl Environ Microbiol. 1998;64(6):2247–2255. doi: 10.1128/AEM.64.6.2247-2255.1998 |
| [74] |
Christensen B.B., Sternberg C., Andersen J.B., et al. Establishment of new genetic traits in a microbial biofilm community. Appl Environ Microbiol. 1998. Vol. 64, N 6. P. 2247–2255. doi: 10.1128/AEM.64.6.2247-2255.1998 |
| [75] |
Gorbakov VV, Hazanov AI, Blohina IP, et al. Natural course of combined hepatitis B and C [Estestvennoe techenie sochetannykh gepatitov В i С]. Clinical Microbiology and Antimicrobial Chemotherapy. 2003;3(3):21–23. (In Russ). |
| [76] |
Горбаков В.В., Хазанов А.И., Блохина И.П., и др. Естественное течение сочетанных гепатитов В и С // Клиническая микробиология и антимикробная химиотерапия. 2003. Т. 3, № 3. С. 209–214. |
| [77] |
Yakovlev AA, Savilov ED. Problematic issues of General epidemiology. Novosibirsk: Nauka; 2015. (In Russ). |
| [78] |
Яковлев А.А., Савилов Е.Д. Проблемные вопросы общей эпидемиологии. Новосибирск : Наука, 2015. |
| [79] |
Bai L, Zhao Y, Dong J, et al. Co-infection of influenza A virus enhances SARS-CoV-2 infectivity. bioRxiv. 2020;(2020):10.14.335893. doi: 10.1101/2020.10.14.335893 |
| [80] |
Bai L., Zhao Y., Dong J., et al. Co-infection of influenza A virus enhances SARS-CoV-2 infectivity. bioRxiv. 2020. N 2020. S. 10.14.335893. doi: 10.1101/2020.10.14.335893 |
| [81] |
Mancini DA, Alves RC, Mendonça RM, et al. Influenza virus and proteolytic bacteria co-infection in respiratory tract from individuals presenting respiratory manifestations. Rev Inst Med Trop Sao Paulo. 2008;50(1):41–46. doi: 10.1590/s0036-46652008000100009 |
| [82] |
Mancini D.A., Alves R.C., Mendonça R.M., et al. Influenza virus and proteolytic bacteria co-infection in respiratory tract from individuals presenting respiratory manifestations. Rev Inst Med Trop Sao Paulo. 2008. Vol. 50, N 1. Р. 41–46. doi: 10.1590/s0036-46652008000100009 |
| [83] |
Dubrovina TYa, Grabovskaya KB, Ivanova IA. Lethal synergy of virus-bacterial infections (model: influenza-Streptococcus) [Letal’nyi sinergizm virus-bakterial’nykh infektsii (model’: gripp-streptokokk)]. Annals of the Russian Academy of medical sciences. 1989;(11):17–22. (In Russ). |
| [84] |
Дубровина Т.Я., Грабовская К.Б., Иванова И.А. Летальный синергизм вирус-бактериальных инфекций (модель: грипп-стрептококк) // Вестник Академии медицинских наук СССР. 1989. № 11. С. 17–22. |
| [85] |
Hahm B, Arbour N, Oldstone MB. Measles virus interacts with human SLAM receptor on dendritic cells to cause immunosuppression. Virology. 2004;323(2):292–302. doi: 10.1016/j.virol.2004.03.011 |
| [86] |
Hahm B., Arbour N., Oldstone M.B. Measles virus interacts with human SLAM receptor on dendritic cells to cause immunosuppression. Virology. 2004. Vol. 323, N 2. P. 292–302. doi: 10.1016/j.virol.2004.03.011 |
| [87] |
Servet-Delprat C, Vidalain PO, Bausinger H, et al. Measles virus induces abnormal differentiation of CD40 ligand-activated human dendritic cells. J Immunol. 2000;164(4):1753–1760. doi: 10.4049/jimmunol.164.4.1753 |
| [88] |
Servet-Delprat C., Vidalain P.O., Bausinger H., et al. Measles virus induces abnormal differentiation of CD40 ligand-activated human dendritic cells. J Immunol. 2000. Vol. 164, N 4. P. 1753–1760. doi: 10.4049/jimmunol.164.4.1753 |
| [89] |
Slifka MK, Homann D, Tishon A, et al. Measles virus infection results in suppression of both innate and adaptive immune responses to secondary bacterial infection. J Clin Invest. 2003;111(6):805–810. doi: 10.1172/JCI13603 |
| [90] |
Slifka M.K., Homann D., Tishon A., et al. Measles virus infection results in suppression of both innate and adaptive immune responses to secondary bacterial infection. J Clin Invest. 2003. Vol. 111, N 6. P. 805–810. doi: 10.1172/JCI13603 |
| [91] |
Barton ES, White DW, Cathelyn JS, et al. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature. 2007;447(7142):326−329. doi: 10.1038/nature05762 |
| [92] |
Barton E.S., White D.W., Cathelyn J.S., et al. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature. 2007. Vol. 447, N 7142. P. 326−329. doi: 10.1038/nature05762 |
| [93] |
Kuss SK, Best GT, Etheredge CA, et al. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science. 2011;334(6053):249–252. doi: 10.1126/science.1211057 |
| [94] |
Kuss S.K., Best G.T., Etheredge C.A., et al. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science. 2011. Vol. 334, N 6053. P. 249–252. doi: 10.1126/science.1211057 |
| [95] |
Ichinohe T, Pang IK, Kumamoto Y, et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci USA. 2011;108(13):5354–5359. doi: 10.1073/pnas.1019378108 |
| [96] |
Ichinohe T., Pang I.K., Kumamoto Y., et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci USA. 2011. Vol. 108, N 13. P. 5354–5359. doi: 10.1073/pnas.1019378108 |
| [97] |
Wilks J, Golovkina T. Influence of microbiota on viral infections. PLOS Pathog. 2012;8(5):e1002681. doi: 10.1371/journal.ppat.1002681 |
| [98] |
Wilks J., Golovkina T. Influence of microbiota on viral infections. PLOS Pathog. 2012. Vol. 8, N 5. e1002681. doi: 10.1371/journal.ppat.1002681 |
| [99] |
Kuz’min AV. Mikrobiologicheskie i ehpidemiologicheskie osobennosti psevdotuberkuleza v Primorskom krae v sovremennyi period [dissertation abstract]. Vladivostok; 1997. Available from: https://search.rsl.ru/ru/record/01000048905. (In Russ). |
| [100] |
Кузьмин А.В. Микробиологические и эпидемиологические особенности псевдотуберкулеза в Приморском крае в современный период: автореф. дис. ... канд. мед. наук. Владивосток, 1997. Режим доступа: https://search.rsl.ru/ru/record/01000048905. Дата обращения: 12.06.2020. |
| [101] |
Rakov AV, Yakovlev AA, Kuznetsova NA. Interaction of Salmonella enteritidis and Salmonella typhimurium in microbial association formed by them in in vitro experiment. Bull Exp Biol Med. 2019;(7):80–82. doi: 10.1007/s10517-019-04649-z |
| [102] |
Раков А.В., Яковлев А.А, Кузнецова Н.А. Взаимодействие Salmonella enteritidis и Salmonella typhimurium в формируемой ими микробной ассоциации в эксперименте in vitro // Бюллетень экспериментальной биологии и медицины. 2019. № 7. С. 80–82. doi: 10.1007/s10517-019-04649-z |
| [103] |
Faruque SM, Mekalanos JJ. Phage-bacterial interactions in the evolution of toxigenic Vibrio cholerae. Virulence. 2012;3(7):556–565. doi: 10.4161/viru.22351 |
| [104] |
Faruque S.M., Mekalanos J.J. Phage-bacterial interactions in the evolution of toxigenic Vibrio cholerae. Virulence. 2012. Vol. 3, N 7. P. 556–565. doi: 10.4161/viru.22351 |
| [105] |
Høiby N. A short history of microbial biofilms and biofilm infections. APMIS. 2017;125(4):272–275. doi: 10.1111/apm.12686 |
| [106] |
Høiby N. A short history of microbial biofilms and biofilm infections. APMIS. 2017. Vol. 125, N 4. P. 272–275. doi: 10.1111/apm.12686 |
| [107] |
Yang L, Liu Y, Wu H, et al. Current understanding of multi-species biofilms. Int J Oral Sci. 2011;3(2):74–81. doi: 10.4248/IJOS11027 |
| [108] |
Yang L., Liu Y., Wu H., et al. Current understanding of multi-species biofilms. Int J Oral Sci. 2011. Vol. 3, N 2. P. 74–81. doi: 10.4248/IJOS11027 |
| [109] |
Elias S, Banin E. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev. 2012;36(5):990–1004. doi: 10.1111/j.1574-6976.2012.00325.x |
| [110] |
Elias S., Banin E. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev. 2012. Vol. 36, N 5. P. 990–1004. doi: 10.1111/j.1574-6976.2012.00325.x |
| [111] |
Burmølle M, Ren D, Bjarnsholt T, Sorensen SJ. Interactions in multispecies biofilms: do they actually matter? Trends Microbiol. 2014;22(2):84–91. doi: 10.1016/j.tim.2013.12.004 |
| [112] |
Burmølle M., Ren D., Bjarnsholt T., Sorensen S.J. Interactions in multispecies biofilms: do they actually matter? Trends Microbiol. 2014. Vol. 22, N 2. P. 84–91. doi: 10.1016/j.tim.2013.12.004 |
| [113] |
Nadell CD, Xavier JB, Foster KR. The sociobiology of biofilms. FEMS Microbiol Rev. 2009;33(1):206–224. doi: 10.1111/j.1574-6976.2008.00150.x |
| [114] |
Nadell C.D., Xavier J.B., Foster K.R. The sociobiology of biofilms. FEMS Microbiol Rev. 2009. Vol. 33, N 1. P. 206–224. doi: 10.1111/j.1574-6976.2008.00150.x |
| [115] |
Moons P, Michiels CW, Aertsen A. Bacterial interactions in biofilms. Crit Rev Microbiol. 2009;35(3):157–168. doi: 10.1080/10408410902809431 |
| [116] |
Moons P., Michiels C.W., Aertsen A. Bacterial interactions in biofilms. Crit Rev Microbiol. 2009. Vol. 35, N 3. P. 157–168. doi: 10.1080/10408410902809431 |
| [117] |
Timchenko NF, Rakov AV, Terent’eva NA, Jakovlev AA. Characteristic of the mixed bacteria of the Enterobacteriaceae family Yersinia pseudotuberculosis and S. enteritidis in vitro. Zdorov’e. Meditsinskaya ehkologiya. Nauka. 2019;(1):19–22. (In Russ). |
| [118] |
Тимченко Н.Ф., Раков А.В., Терентьева Н.А., Яковлев А.А. Характеристика смешанных биопленок бактерий семейства Enterobacteriaceae Yersinia pseudotuberculosis и Salmonella Enteritidis in vitro // Здоровье. Медицинская экология. Наука. 2019. № 1. С. 19–22. |
| [119] |
Peters BM, Jabra-Rizk MA, O’May GA, et al. Polymicrobial interactions: impact on pathogenesis and human disease. Clin Microbiol Rev. 2012;25(1):193–213. doi: 10.1128/CMR.00013-11 |
| [120] |
Peters B.M., Jabra-Rizk M.A., O’May G.A., et al. Polymicrobial interactions: impact on pathogenesis and human disease. Clin Microbiol Rev. 2012. Vol. 25, N 1. P. 193–213. doi: 10.1128/CMR.00013-11 |
| [121] |
Giaouris E, Chorianopoulos N, Doulgeraki A, Nychas GJ. Co-culture with Listeria monocytogenes within a dual-species biofilm community strongly increases resistance of Pseudomonas putida to benzalkonium chloride. PLoS One. 2013;8(10):e77276. doi: 10.1371/journal.pone.0077276 |
| [122] |
Giaouris E., Chorianopoulos N., Doulgeraki A., Nychas G.J. Co-culture with Listeria monocytogenes within a dual-species biofilm community strongly increases resistance of Pseudomonas putida to benzalkonium chloride. PLoS One. 2013. Vol. 8, N 10. e77276. doi: 10.1371/journal.pone.0077276 |
| [123] |
Lee KW, Periasamy S, Mukherjee M, et al. Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J. 2014;8(4):894–907. doi: 10.1038/ismej.2013.194 |
| [124] |
Lee K.W., Periasamy S., Mukherjee M., et al. Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J. 2014. Vol. 8, N 4. P. 894–907. doi: 10.1038/ismej.2013.194 |
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