Email this article Synergism and antagonism in intestinal microbial communities in closed organized collectives
- Authors: Ermolaev A.V.1, Kaiumov K.A.1, Lyamin A.V.1, Gorbachev D.O.1
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Affiliations:
- Samara State Medical University
- Issue: Vol 15, No 4 (2025)
- Pages: 770-774
- Section: SHORT COMMUNICATIONS
- Submitted: 02.03.2025
- Accepted: 31.07.2025
- Published: 06.11.2025
- URL: https://iimmun.ru/iimm/article/view/17874
- DOI: https://doi.org/10.15789/2220-7619-SAA-17874
- ID: 17874
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Abstract
Introduction. The gut microbiota represents the largest part of the entire human microbiome. The formation of a stable microbiota begins at childbirth, continuing to change during life influenced by various exogenous and hereditary factors. One of such external cues is presented by closed organized collectives, where different individuals, due to the common way of life and nutrition, undergo a restructuring of the intestinal microbial communities. In addition to microbiota quantitative and qualitative changes, inter-microbial communities may also be altered (synergism, antagonism, mutualism). The aim of the study was to analyze the synergistic and antagonistic relationships between intestinal microbial communities in individuals from closed organized collectives.
Materials and methods. The study group included 120 male subjects aged 18 to 22 years, who lived within the same closed organized collectives for 9 months. Fecal samples were selected for plating prior to living in closed organized collectives (stage 1), and 9 months afterwards (stage 2). The identified microorganisms were assigned to the permanent, supplementary, or random microbiota group. To assess the relationship between pairs of genera, the Jaccard index was calculated.
Results. The results of the study showed that the synergistic relationships between members of the permanent microbiota remain stable or increase over time, which generally corresponds to the data on the properties of the obligate microbiota. Positive synergistic relationships with additional microbiota have also been identified, e.g., between Bifidobacterium spp. and the order of Lactobacillales. The synergy of these genera can effectively support normal gastrointestinal tract functioning. However, antagonistic relationships were also noted, especially between some representatives of the additional and permanent microbiota, such as Klebsiella spp. Such data may indicate a negative effect of certain microorganisms on the intestinal microbiota in a limited collective setting.
Conclusion. Further research in this field may help explain changes in microbial communities in organized collectives and develop strategies for healthy microbiota maintenance therein.
Full Text
Inroduction
The gut microbiota make up the largest part of the entire human microbiome and play a crucial role in maintaining healthy homeostasis. Colonization of the gastrointestinal tract by microorganisms and formation of a stable microbiota begin with childbirth and continue to change throughout life under the influence of various external (lifestyle, diet, medications, geographical location) and inherited factors [6, 10]. One of these external factors is the presence in closed organized collectives (for example, in military units), where different individuals, due to the common way of life and changing the diet to the same type, undergo a restructuring of intestinal microbial communities [4, 5, 8, 9]. In addition to quantitative and qualitative changes in the microbiota, there are also changes in the relationships between microbial communities. Synregism and antagonism of various microorganisms can both favorably affect the physiology of the gastrointestinal tract, (for example, antagonism of the intestinal microbiota against pathogens forms colonization resistance) and contribute to the development of pathological processes (for example, the exchange of resistance genes, biofilm formation, etc.) [2, 13].
The aim of this study is to analyze the synergistic and antagonistic relationships of intestinal microbial communities in closed organized collectives.
Materials and methods
The study group included 120 people aged 18 to 22 years, male, who lived within one closed organized collective for 9 months. Feces were collected from participants for sowing before the start of their stay in a closed collective (stage 1 of the study), and 9 months after (stage 2 of the study). The study was approved by the Bioethics Committee at Samara State Medical University (protocol No. 252 dated 09/07/2022). Collection and transportation of biomaterial for microbiological research was carried out in accordance with Methodological Guidelines 4.2.2039-05 “Technique for collecting and transporting biomaterials to microbiological laboratories”. The biomaterial was sowed under anaerobic conditions using a Bactron 300-2 anaerobic station (Sheldon Manufacturing Inc., USA) on an extended range of nutrient media: MacConkey agar (HiMedia, India), Veillonella agar (HiMedia, India), Clostridium agar (Condalab, Spain), Bifidobacterium agar (HiMedia, India), Anaerobic agar (HiMedia, India), Brucella agar (HiMedia, India), Muller–Hinton agar with 5% sheep blood (HiMedia, India), chromogenic agar (HiMedia, India), Lactobacillus agar (Condalab, Spain), Saburo agar (HiMedia, India). Cultivation was carried out at a temperature of 37°C for 120 hours. The cultures were identified by MALDI-ToF mass spectrometry using a “MicroflexLT” instrument (Bruker, Germany). For all identified microorganisms, the coefficient of constancy (C) was calculated, depending on which they were assigned to the group of constant (C > 50%), additional (25% < C > 50%) or random (C < 25%) microbiota [3]. To assess the relationship between pairs of genera belonging to permanent and additional microorganisms, the Jaccard index (q) was calculated, depending on which relationship was evaluated as antagonism (q ≤ 30%), synergy (q = 30–70%) or mutualism (q ≥ 70%) [3]. Statistical analysis was carried out using the StatTech v. 4.6.3 program (developer — StatTech LLC, Russia). Categorical data were described using absolute values and percentages. Quantitative indicators with normal distribution were described using arithmetic means (M) and standard deviations (SD), 95% confidence interval limits (95% CI). In the absence of normal distribution, quantitative data were described using the median (Me) and lower and upper quartiles (Q1–Q3).
Results and discussion
As a result of the study, the permanent intestinal microbiota at the first stage included the following microorganisms: Aspergillus spp. (52.5%), Enterococcus spp. (84.2%), Escherichia spp. (100%), Lactobacillus spp. (61.7%). At the second stage, it included: Enterococcus spp. (85.8%), Escherichia spp. (100%), Klebsiella spp. (55%), Lactobacillus spp. (53.3%), Staphylococcus spp. (65%), Streptococcus spp. (53.3%).
Pairs were identified to compare the constant gut microbiota. The results of calculating the Jaccard index for pairs of constant microbiota are presented in Table 1.
Table 1. The results of calculating the Jaccard index for pairs of constant microbiota
Pair | Research stage | a* | b** | c*** | q**** | Relationship direction |
Aspergillus spp. + Escherichia spp. | Stage 1 | 63 | 120 | 63 | 52.5 | Synergism |
Stage 2 | 53 | 120 | 53 | 44.1 | Synergism | |
Aspergillus spp. + Enterococсus spp. | Stage 1 | 63 | 101 | 54 | 49.0 | Synergism |
Stage 2 | 53 | 103 | 46 | 41.8 | Synergism | |
Aspergillus spp. + Lactobacillus spp. | Stage 1 | 63 | 74 | 39 | 39.8 | Synergism |
Stage 2 | 53 | 64 | 25 | 27.1 | Antagonism | |
Escherichia spp. + Staphylococcus spp. | Stage 1 | 120 | 29 | 29 | 24.1 | Antagonism |
Stage 2 | 120 | 78 | 78 | 65.0 | Synergism | |
Enterococсus spp. + Staphylococcus spp. | Stage 1 | 101 | 29 | 24 | 22.6 | Antagonism |
Stage 2 | 103 | 78 | 68 | 60.1 | Synergism | |
Klebsiella spp. + Staphylococcus spp. | Stage 1 | 59 | 29 | 13 | 17.3 | Antagonism |
Stage 2 | 66 | 78 | 42 | 41.1 | Synergism | |
Lactobacillus spp. + Staphylococcus spp. | Stage 1 | 74 | 29 | 16 | 18.39 | Antagonism |
Stage 2 | 64 | 78 | 49 | 52.69 | Synergism | |
Staphylococcus spp. + Streptococcus spp. | Stage 1 | 29 | 40 | 8 | 13.11 | Antagonism |
Stage 2 | 78 | 64 | 45 | 46.39 | Synergism |
Note. *a — the number of subjects from whom the first microorganism was isolated; **b — the number of subjects from whom the second microorganism was isolated; ***с — the number of subjects in whom both microorganisms were isolated from the corresponding pair; ****q — Jaccard index.
As a result of the study, the following microorganisms were included in the additional intestinal microbiota at the first stage: Bacillus spp. (30%), Bifidobacterium spp. (43.3%), Citrobacter spp. (32.5%), Klebsiella spp. (49.2%), Lactococcus spp. (25.8%), Streptococcus spp. (33.3%). At the second stage, it included: Aspergillus spp. (44.2%), Bifidobacterium spp. (48.3%), Citrobacter spp. (25.8%), Clostridium spp. (25%), Lacticaseibacillus spp. (40.8%), Ligilactobacillus spp. (29.2%), Limosilactobacillus spp. (29.2%), Micrococcus spp. (35%), Pseudomonas spp. (25.8%).
Pairs were identified to compare the additional gut microbiota. The results of calculating the Jaccard index for pairs of additional microbiota are presented in Table 2.
Table 2. The results of calculating the Jaccard index for pairs of additional microbiota
Pair | Research stage | a* | b** | c*** | q**** | Relationship direction |
Bacillus spp. + Klebsiella spp. | Stage 1 | 36 | 59 | 18 | 23.38 | Synergism |
Stage 2 | 20 | 66 | 12 | 16.22 | Antagonism | |
Bifidobacterium spp. + Klebsiella spp. | Stage 1 | 52 | 59 | 22 | 24.72 | Antagonism |
Stage 2 | 58 | 66 | 37 | 42.53 | Synergism | |
Bifidobacterium spp. + Ligilactobacillus spp. | Stage 1 | 52 | 0 | 0 | 0.00 | Antagonism |
Stage 2 | 58 | 35 | 22 | 30.99 | Synergism | |
Bifidobacterium spp. + Limosilactobacillus spp. | Stage 1 | 52 | 0 | 0 | 0.00 | Antagonism |
Stage 2 | 58 | 35 | 22 | 30.99 | Synergism | |
Bifidobacterium spp. + Streptococcus spp. | Stage 1 | 52 | 40 | 18 | 24.32 | Antagonism |
Stage 2 | 58 | 64 | 35 | 40.23 | Synergism | |
Citrobacter spp. + Klebsiella spp. | Stage 1 | 39 | 59 | 25 | 34.25 | Synergism |
Stage 2 | 31 | 66 | 18 | 22.78 | Antagonism | |
Klebsiella spp. + Lactococcus spp. | Stage 1 | 18 | 31 | 20 | 68.97 | Synergism |
Stage 2 | 66 | 22 | 18 | 25.71 | Antagonism | |
Klebsiella spp. + Streptococcus spp. | Stage 1 | 18 | 40 | 24 | 70.59 | Mutualism |
Stage 2 | 66 | 64 | 40 | 44.44 | Synergism | |
Lacticaseibacillus spp. + Limosilactobacillus spp. | Stage 1 | 0 | 0 | 0 | 0.0 | Antagonism |
Stage 2 | 49 | 35 | 20 | 31.2 | Synergism | |
Ligilactobacillus spp. + Pseudomonas spp. | Stage 1 | 0 | 12 | 0 | 0.0 | Antagonism |
Stage 2 | 35 | 31 | 16 | 32.0 | Synergism | |
Aspergillus spp. + Micrococcus spp. | Stage 1 | 63 | 25 | 10 | 12.8 | Antagonism |
Stage 2 | 53 | 42 | 24 | 33.8 | Synergism |
Note. *a — the number of subjects from whom the first microorganism was isolated; **b — the number of subjects from whom the second microorganism was isolated; ***с — the number of subjects in whom both microorganisms were isolated from the corresponding pair; ****q — Jaccard index.
The study revealed both synergistic and antagonistic relationships between representatives of the intestinal microbiota in individuals forming an organized closed-type team.
Pairs of Aspergillus spp. + Escherichia spp. and Aspergillus spp. + Enterococcus spp. at the first stage, they have a high synergistic relationship, but at the 2nd stage of the study, this relationship is suppressed and turns into an antagonistic one. It can be assumed that this is due to the pronounced negative effect of Aspergillus spp. A similar situation can be noted in the pair Aspergillus spp. + Lactobacillus spp., where synergy has turned into antagonism. For pairs of representatives of the order Enterobacterales, 100% synergy can be noted in the 2nd stage of the study in comparison with the 1st. Also worth noting is the pair Escherichia spp. + Enterococсus spp. with a coefficient of 84.1% at the 1st stage of the study, corresponding to mutualism, followed by an increase in this relationship at the 2nd stage of the study to 85.8%.
Pairs of additional gut microbiota with a high level of synergy were analyzed. Pairs of Bifidobacterium spp. + Lacticaseibacillus spp. and Bifidobacterium spp. + Ligilactobacillus spp. at the 1st stage of the study, when forming an organized closed-type team, they are defined as antagonists, but at the 2nd stage of the study, the presented pairs are defined as synergists. A similar behavior can be observed between pairs of Bifidobacterium spp. + Klebsiella spp., Bifidobacterium spp. + Streptococcus spp., Lacticaseibacillus spp. + Limosilactobacillus spp., Ligilactobacillus spp. + Pseudomonas spp.
A pair of Bacillus spp. + Klebsiella spp. at the 1st stage of the study, it was defined as synergistic, but at the 2nd stage, the transition of communication in favor of antagonism is noted. A similar situation can be observed between pairs such as Citrobacter spp. + Klebsiella spp., Klebsiella spp. + Lactococcus spp.
Thus, the results of the study showed that the synergistic relationships between representatives of the permanent microbiota remain stable or increase over time, which generally corresponds to the data on the properties of the obligate microbiota [7, 11]. Positive synergistic relationships with additional microbiota have also been identified, for example between Bifidobacterium spp. and the order of Lactobacillales. The synergy of these genera can effectively support the normal functioning of the gastrointestinal tract, which is widely used in the production of probiotics [1]. However, antagonistic relationships were also noted, especially between some representatives of the additional and permanent microbiota, such as Klebsiella spp. In recent years, the ability to antagonize the latter has been widely discussed in the scientific community [12]. Such data may indicate a negative effect of certain microorganisms on the intestinal microbiota in closed collectives.
Additional data are needed to better understand the synergistic and antagonistic relationships between representatives of the gut microbiota. Further research in this area will help explain the dynamics of changes in microbial communities in organized collectives and develop strategies for maintaining a healthy microbiota in such conditions.
About the authors
A. V. Ermolaev
Samara State Medical University
Email: k.a.kayumov@samsmu.ru
Assistant Professor, Department of General Hygiene
Россия, SamaraK. A. Kaiumov
Samara State Medical University
Author for correspondence.
Email: k.a.kayumov@samsmu.ru
Specialist of the Research and Educational Professional Center for Genetic and Laboratory Technologies
Россия, SamaraA. V. Lyamin
Samara State Medical University
Email: k.a.kayumov@samsmu.ru
DSc (Medicine), Associate Professor, Director of the Research and Educational Professional Center for Genetic and Laboratory Technologies
Россия, SamaraD. O. Gorbachev
Samara State Medical University
Email: k.a.kayumov@samsmu.ru
DSc (Medicine), Associate Professor, Head of the Department of General Hygiene
Россия, SamaraReferences
- Андреева И.В., Стецюк О.У. Эффективность и безопасность комбинации Lactobacillus acidophilus La-5 и Bifidobacterium lactis Вb-12 в гастроэнтерологии, педиатрии и аллергологии // Клиническая микробиология и антимикробная химиотерапия. 2016. Т. 18, № 2. С. 113–124. [Andreeva I.V., Stetsiouk O.U. Efficacy and Safety of Lactobacillus acidophilus LA5 and Bifidobacterium lactis BB12 Combination in Gastroenterology, Pediatrics and Allergology. Klinicheskaya mikrobiologiya i antimikrobnaya khimioterapiya = Clinical Microbiology and Antimicrobial Chemotherapy, 2016, vol. 18, no. 2, pp. 113–124. (In Russ.)]
- Бекпергенова А.В., Хлопко Ю.А., Иванова Е.В., Перунова Н.Б. Формирование ассоциаций облигатно-анаэробных бактерий толстого кишечника человека // Вестник Оренбургского государственного университета. 2017. Т. 9, № 209. С. 51–56. [Bekpergenova A.V., Khlopko Yu.A., Ivanova E.V., Perunova N.B. Formation of associations of obligate anaerobic bacteria of the human large intestine. Vestnik Orenburgskogo gosudarstvennogo universiteta = Bulletin of the Orenburg State University, 2017, vol. 9, no. 209, pp. 51–56. (In Russ.)]
- Немченко У.М., Савелькаева М.В., Ракова Е.Б., Иванова Е.И., Сердюк Л.В. Микроэкологическая характеристика кишечного биоценоза у детей с функциональными нарушениями желудочно-кишечного тракта // Клиническая лабораторная диагностика. 2016. Т. 61, № 6. С. 368–371. [Nemtchenko U.M., Savelkaieva M.V., Rakova E.B., Ivanova E.I., Serdyuk L.V. The microecological characteristic of intestinal biocenosis of children with functional disorders of gastrointestinal tract. Klinicheskaya laboratornaya diagnostika = Russian Clinical Laboratory Diagnostics, 2016, vol. 61, no 6, pp. 368–371. (In Russ.)] doi: 10.18821/0869-2084-2016-61-6-368-371
- Bibbò S., Ianiro G., Giorgio V., Scaldaferri F., Masucci L., Gasbarrini A., Cammarota G. The role of diet on gut microbiota composition. Eur. Rev. Med. Pharmacol. Sci., 2016, vol. 20, no. 22, pp. 4742–4749.
- Fan L., Xia Y., Wang Y., Han D., Liu Y., Li J., Fu J., Wang L., Gan Z., Liu B., Fu J., Zhu C., Wu Z., Zhao J., Han H., Wu H., He Y., Tang Y., Zhang Q., Wang Y., Zhang F., Zong X., Yin J., Zhou X., Yang X., Wang J., Yin Y., Ren W. Gut microbiota bridges dietary nutrients and host immunity. Sci. China Life Sci., 2023, vol. 66, no. 11, pp. 2466–2514. doi: 10.1007/s11427-023-2346-1
- Jung Y., Tagele S.B., Son H., Ibal J.C., Kerfahi D., Yun H., Lee B., Park C.Y., Kim E.S., Kim S.J., Shin J.H. Modulation of Gut Microbiota in Korean Navy Trainees following a Healthy Lifestyle Change. Microorganisms, 2020, vol. 8, no. 9: 1265. doi: 10.3390/microorganisms8091265
- Nava G.M., Stappenbeck T.S. Diversity of the autochthonous colonic microbiota. Gut Microbes, 2011, vol. 2, no. 2, pp. 99–104. doi: 10.4161/gmic.2.2.15416
- Valdes A.M., Walter J., Segal E., Spector T.D. Role of the gut microbiota in nutrition and health. BMJ, 2018, vol. 361: k2179. doi: 10.1136/bmj.k2179
- Valles-Colomer M., Blanco-Míguez A., Manghi P., Asnicar F., Dubois L., Golzato D., Armanini F., Cumbo F., Huang K.D., Manara S., Masetti G., Pinto F., Piperni E., Punčochář M., Ricci L., Zolfo M., Farrant O., Goncalves A., Selma-Royo M., Binetti A.G., Becerra J.E., Han B., Lusingu J., Amuasi J., Amoroso L., Visconti A., Steves C.M., Falchi M., Filosi M., Tett A., Last A., Xu Q., Qin N., Qin H., May J., Eibach D., Corrias M.V., Ponzoni M., Pasolli E., Spector T.D., Domenici E., Collado M.C., Segata N. The person-to-person transmission landscape of the gut and oral microbiomes. Nature, 2023, vol. 614, no. 7946, pp. 125–135. doi: 10.1038/s41586-022-05620-1
- Van Hul M., Cani P.D., Petitfils C., De Vos W.M., Tilg H., El-Omar E.M. What defines a healthy gut microbiome? Gut, 2024, vol. 73, no. 11, pp. 1893–1908. doi: 10.1136/gutjnl-2024-333378
- Vos M. Accessory microbiomes. Microbiology (Reading), 2023, vol. 169, no. 5: 001332. doi: 10.1099/mic.0.001332
- Zechner E.L., Kienesberger S. Microbiota-derived small molecule genotoxins: host interactions and ecological impact in the gut ecosystem. Gut Microbes, 2024, vol. 16, no. 1: 2430423. doi: 10.1080/19490976.2024.2430423
- Zhang Y., Tan P., Zhao Y., Ma X. Enterotoxigenic Escherichia coli: intestinal pathogenesis mechanisms and colonization resistance by gut microbiota. Gut Microbes, 2022, vol. 14, no. 1: 2055943. doi: 10.1080/19490976.2022.2055943
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