Natural History and Ecology of Interactions Between Bordetella Species and Amoeba

被引:6
|
作者
Ma, Longhuan [1 ]
Linz, Bodo [1 ,2 ]
Caulfield, Amanda D. [1 ]
Dewan, Kalyan K. [1 ]
Rivera, Israel [1 ]
Harvill, Eric T. [1 ]
机构
[1] Univ Georgia, Coll Vet Med, Dept Infect Dis, Athens, GA 30602 USA
[2] Friedrich Alexander Univ Erlangen Nuremberg, Div Microbiol, Dept Biol, Erlangen, Germany
来源
FRONTIERS IN CELLULAR AND INFECTION MICROBIOLOGY | 2022年 / 12卷
基金
美国国家卫生研究院;
关键词
Bordetella species; Dictyostelium discoideum; interactions; evolution; GWAS -genome-wide association study; RESPIRATORY EPITHELIAL-CELLS; SP-NOV; INTRACELLULAR SURVIVAL; PERTUSSIS; INVASION; PHAGOCYTOSIS; INFECTIONS; SEQUENCES; TOXIN;
D O I
10.3389/fcimb.2022.798317
中图分类号
R392 [医学免疫学]; Q939.91 [免疫学];
学科分类号
100102 ;
摘要
A variety of bacteria have evolved the ability to interact with environmental phagocytic predators such as amoebae, which may have facilitated their subsequent interactions with phagocytes in animal hosts. Our recent study found that the animal pathogen Bordetella bronchiseptica can evade predation by the common soil amoeba Dictyostelium discoideum, survive within, and hijack its complex life cycle as a propagation and dissemination vector. However, it is uncertain whether the mechanisms allowing interactions with predatory amoebae are conserved among Bordetella species, because divergence, evolution, and adaptation to different hosts and ecological niches was accompanied by acquisition and loss of many genes. Here we tested 9 diverse Bordetella species in three assays representing distinct aspects of their interactions with D. discoideum. Several human and animal pathogens retained the abilities to survive within single-celled amoeba, to inhibit amoebic plaque expansion, and to translocate with amoebae to the fruiting body and disseminate along with the fruiting body. In contrast, these abilities were partly degraded for the bird pathogen B. avium, and for the human-restricted species B. pertussis and B. parapertussis. Interestingly, a different lineage of B. parapertussis only known to infect sheep retained the ability to interact with D. discoideum, demonstrating that these abilities were lost in multiple lineages independently, correlating with niche specialization and recent rapid genome decay apparently mediated by insertion sequences. B. petrii has been isolated sporadically from diverse human and environmental sources, has acquired insertion sequences, undergone genome decay and has also lost the ability to interact with amoebae, suggesting some specialization to some unknown niche. A genome-wide association study (GWAS) identified a set of genes that are potentially associated with the ability to interact with D. discoideum. These results suggest that massive gene loss associated with specialization of some Bordetella species to a closed life cycle in a particular host was repeatedly and independently accompanied by loss of the ability to interact with amoebae in an environmental niche.
引用
收藏
页数:12
相关论文
共 50 条
  • [21] The natural history of Nicrophorus nigrita, a western Nearctic species (Coleoptera: Silphidae)
    Sikes, DS
    PAN-PACIFIC ENTOMOLOGIST, 1996, 72 (02) : 70 - 81
  • [22] Interactions between ecosystem engineers: A native species indirectly facilitates a non-native one
    Cruz Sueiro, Maria
    Schwindt, Evangelina
    Mendez, Maria Martha
    Bortolus, Alejandro
    ACTA OECOLOGICA-INTERNATIONAL JOURNAL OF ECOLOGY, 2013, 51 : 11 - 16
  • [23] Effects of fluid flow conditions on interactions between species in biofilms
    Zhang, Wei
    Sileika, Tadas
    Packman, Aaron I.
    FEMS MICROBIOLOGY ECOLOGY, 2013, 84 (02) : 344 - 354
  • [24] Interactions between reactive oxygen and nitrogen species in inflammatory neurodegeneration
    Brown, G. C.
    FREE RADICAL BIOLOGY AND MEDICINE, 2012, 53 : S29 - S30
  • [25] Not just females: the socio-ecology of social interactions between spider monkey males
    Aline Saldana-Sanchez, Amor
    Schaffner, Colleen M.
    Smith-Aguilar, Sandra
    Aureli, Filippo
    PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2022, 289 (1978)
  • [26] Habitat and life history differences between two species of Gambusia
    Swenton, Daniella M.
    Kodric-Brown, Astrid
    ENVIRONMENTAL BIOLOGY OF FISHES, 2012, 94 (04) : 669 - 680
  • [27] Genetic Interactions Between Transcription Factors Cause Natural Variation in Yeast
    Gerke, Justin
    Lorenz, Kim
    Cohen, Barak
    SCIENCE, 2009, 323 (5913) : 498 - 501
  • [28] Maternal experience and soil origin influence interactions between resident species and a dominant invasive species
    Gisela C. Stotz
    Ernesto Gianoli
    James F. Cahill
    Oecologia, 2018, 186 : 247 - 257
  • [29] Maternal experience and soil origin influence interactions between resident species and a dominant invasive species
    Stotz, Gisela C.
    Gianoli, Ernesto
    Cahill, James F., Jr.
    OECOLOGIA, 2018, 186 (01) : 247 - 257
  • [30] Natural history matters: how biological constraints shape diversified interactions in pollination networks
    Jordano, Pedro
    JOURNAL OF ANIMAL ECOLOGY, 2016, 85 (06) : 1423 - 1426