The Isolation of Culturable Bacteria in Ixodes ricinus Ticks of a Belgian Peri-Urban Forest Uncovers Opportunistic Bacteria Potentially Important for Public Health

Rousseau, Raphaël; Vanwambeke, Sophie; Boland, Cécile; Mori, Marcella

doi:10.3390/ijerph182212134

Cited by 7 publications

(4 citation statements)

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“…Interestingly, this is in contrast to the highly abundant aerobic culturable gut microbiota of other blood-feeding arthropods, such as mosquitoes, analyzed under comparable cultivation conditions used in the current study [ 1 – 3 ]. It is also noteworthy that the majority of the culturable bacteria in the midgut of different tick species tend to be Gram-positive taxa [ 27 , 30 , 33 ].…”

Section: Discussionmentioning

confidence: 99%

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Characterization and manipulation of the bacterial community in the midgut of Ixodes ricinus

et al. 2022

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Background Ticks are obligate hematophagous arthropods transmitting a wide range of pathogens to humans and animals. They also harbor a non-pathogenic microbiota, primarily in the ovaries and the midgut. In the previous study on Ixodes ricinus, we used a culture-independent approach and showed a diverse but quantitatively poor midgut bacterial microbiome. Our analysis also revealed the absence of a core microbiome, suggesting an environmental origin of the tick midgut microbiota. Methods A bacterial analysis of the midgut of adult females collected by flagging from two localities in the Czech Republic was performed. Using the culture-independent approach, we tested the hypothesis that the midgut microbiome is of the environmental origin. We also cultured indigenous bacteria from the tick midgut and used these to feed ticks artificially in an attempt to manipulate the midgut microbiome. Results The midgut showed a very low prevalence and abundance of culturable bacteria, with only 37% of ticks positive for bacteria. The culture-independent approach revealed the presence of Borrelia sp., Spiroplasma sp., Rickettsia sp., Midichloria sp. and various mainly environmental Gram-positive bacterial taxa. The comparison of ticks from two regions revealed that the habitat influenced the midgut bacterial diversity. In addition, the midgut of ticks capillary fed with the indigenous Micrococcus luteus (Gram-positive) and Pantoea sp. (Gram-negative) could not be colonized due to rapid and effective clearance of both bacterial taxa. Conclusions The midgut microbiome of I. ricinus is diverse but low in abundance, with the exception of tick-borne pathogens and symbionts. The environment impacts the diversity of the tick midgut microbiome. Ingested extracellular environmental bacteria are rapidly eliminated and are not able to colonize the gut. We hypothesize that bacterial elimination triggered in the midgut of unfed adult females is critical to maintain low microbial levels during blood-feeding. Graphical Abstract

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Section: Discussionmentioning

confidence: 99%

“…Microccocus luteus is commonly found in soil, water and other environments, and it is also part of the mammalian skin microbiota. In other studies, M. luteus was cultured from I. ricinus in larvae [ 27 ] and nymphs [ 25 ]. Interestingly, Micrococcus spp.…”

Section: Discussionmentioning

confidence: 99%

Characterization and manipulation of the bacterial community in the midgut of Ixodes ricinus

et al. 2022

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“…I. ricinus is widely distributed across Europe. Its existence has been recorded in countries such as the UK, Germany, Sweden, Ukraine, Russia, Italy, France, Spain, Romania, Belgium, Austria, Latvia, and Lithuania [ 20 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 ]. It is also found in Greece and particularly in Northwestern Greece and Crete, according to the current ECDC map distribution for Europe in March 2021 [ 35 , 36 ].…”

Section: How Climate Affects Tick Phenology—the Example Of ...mentioning

confidence: 99%

Climate Changes Exacerbate the Spread of Ixodes ricinus and the Occurrence of Lyme Borreliosis and Tick-Borne Encephalitis in Europe—How Climate Models Are Used as a Risk Assessment Approach for Tick-Borne Diseases

Voyiatzaki

Papailia

Venetikou

et al. 2022

IJERPH

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Climate change has influenced the transmission of a wide range of vector-borne diseases in Europe, which is a pressing public health challenge for the coming decades. Numerous theories have been developed in order to explain how tick-borne diseases are associated with climate change. These theories include higher proliferation rates, extended transmission season, changes in ecological balances, and climate-related migration of vectors, reservoir hosts, or human populations. Changes of the epidemiological pattern have potentially catastrophic consequences, resulting in increasing prevalence of tick-borne diseases. Thus, investigation of the relationship between climate change and tick-borne diseases is critical. In this regard, climate models that predict the ticks’ geographical distribution changes can be used as a predicting tool. The aim of this review is to provide the current evidence regarding the contribution of the climatic changes to Lyme borreliosis (LB) disease and tick-borne encephalitis (TBE) and to present how computational models will advance our understanding of the relationship between climate change and tick-borne diseases in Europe.

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“…Despite a diet limited to the host blood, the tick microbiome appears to be quite complex ( Carpi et al., 2011 ; Pollet et al., 2020 ; Narasimhan et al., 2021 ; Rousseau et al., 2021 ; Kumar et al., 2022a ). Tick microbial communities were found to include tick-borne pathogens causing diseases in humans and animals (viruses, bacteria, protozoa) or pathogens and parasites that infect ticks (microsporidia, fungi, nematodes, hymenopteran parasitoids), and non-pathogenic microorganisms such as commensals or endosymbiotic, mutualistic microbes comprising mainly bacteria.…”

Section: Introductionmentioning

confidence: 99%

What do we know about the microbiome of I. ricinus?

Hodosi

Kazimírová

Šoltýs

2022

Front. Cell. Infect. Microbiol.

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I. ricinus is an obligate hematophagous parasitic arthropod that is responsible for the transmission of a wide range of zoonotic pathogens including spirochetes of the genus Borrelia, Rickettsia spp., C. burnetii, Anaplasma phagocytophilum and Francisella tularensis, which are part the tick´s microbiome. Most of the studies focus on “pathogens” and only very few elucidate the role of “non-pathogenic” symbiotic microorganisms in I. ricinus. While most of the members of the microbiome are leading an intracellular lifestyle, they are able to complement tick´s nutrition and stress response having a great impact on tick´s survival and transmission of pathogens. The composition of the tick´s microbiome is not consistent and can be tied to the environment, tick species, developmental stage, or specific organ or tissue. Ovarian tissue harbors a stable microbiome consisting mainly but not exclusively of endosymbiotic bacteria, while the microbiome of the digestive system is rather unstable, and together with salivary glands, is mostly comprised of pathogens. The most prevalent endosymbionts found in ticks are Rickettsia spp., Ricketsiella spp., Coxiella-like and Francisella-like endosymbionts, Spiroplasma spp. and Candidatus Midichloria spp. Since microorganisms can modify ticks’ behavior, such as mobility, feeding or saliva production, which results in increased survival rates, we aimed to elucidate the potential, tight relationship, and interaction between bacteria of the I. ricinus microbiome. Here we show that endosymbionts including Coxiella-like spp., can provide I. ricinus with different types of vitamin B (B2, B6, B7, B9) essential for eukaryotic organisms. Furthermore, we hypothesize that survival of Wolbachia spp., or the bacterial pathogen A. phagocytophilum can be supported by the tick itself since coinfection with symbiotic Spiroplasma ixodetis provides I. ricinus with complete metabolic pathway of folate biosynthesis necessary for DNA synthesis and cell division. Manipulation of tick´s endosymbiotic microbiome could present a perspective way of I. ricinus control and regulation of spread of emerging bacterial pathogens.

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The Isolation of Culturable Bacteria in Ixodes ricinus Ticks of a Belgian Peri-Urban Forest Uncovers Opportunistic Bacteria Potentially Important for Public Health

Cited by 7 publications

References 46 publications

Characterization and manipulation of the bacterial community in the midgut of Ixodes ricinus

Characterization and manipulation of the bacterial community in the midgut of Ixodes ricinus

Climate Changes Exacerbate the Spread of Ixodes ricinus and the Occurrence of Lyme Borreliosis and Tick-Borne Encephalitis in Europe—How Climate Models Are Used as a Risk Assessment Approach for Tick-Borne Diseases

What do we know about the microbiome of I. ricinus?

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