Intracellular pathogenic bacteria and fungi — a case of convergent evolution?

ABSTRACT The bacterium _Yersinia pestis_ and the fungus _Cryptococcus neoformans_ are the causative agents of human plague and cryptococcosis, respectively. Both microorganisms are

facultatively intracellular pathogens. A comparison of their pathogenic strategies reveals similar tactics for intracellular survival in _Y. pestis_ and _C. neoformans_ despite their genetic

unrelatedness. Both organisms can survive in environments where they are vulnerable to predation by amoeboid protozoal hosts. Here, we propose that the overall similarities in their

pathogenic strategies are an example of convergent evolution that has solved the problem of intracellular survival. Access through your institution Buy or subscribe This is a preview of

subscription content, access via your institution ACCESS OPTIONS Access through your institution Subscribe to this journal Receive 12 print issues and online access $209.00 per year only

$17.42 per issue Learn more Buy this article * Purchase on SpringerLink * Instant access to full article PDF Buy now Prices may be subject to local taxes which are calculated during checkout

ADDITIONAL ACCESS OPTIONS: * Log in * Learn about institutional subscriptions * Read our FAQs * Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS HOST ASSOCIATION AND

INTRACELLULARITY EVOLVED MULTIPLE TIMES INDEPENDENTLY IN THE _RICKETTSIALES_ Article Open access 06 February 2024 EVOLUTION OF THE HUMAN PATHOGENIC LIFESTYLE IN FUNGI Article 04 May 2022

PHENOTYPIC AND GENOMIC HALLMARKS OF A NOVEL, POTENTIALLY PATHOGENIC RAPIDLY GROWING _MYCOBACTERIUM_ SPECIES RELATED TO THE _MYCOBACTERIUM FORTUITUM_ COMPLEX Article Open access 21 June 2021

REFERENCES * Harb, O. S., Gao, L. Y. & Abu Kwaik, Y. From protozoa to mammalian cells: a new paradigm in the life cycle of intracellular bacterial pathogens. _Environ. Microbiol._ 2,

251–265 (2000). Article  CAS  PubMed  Google Scholar  * Solomon, J. M. & Isberg, R. R. Growth of _Legionella pneumophila_ in _Dictyostelium discoideum_: a novel system for genetic

analysis of host–pathogen interactions. _Trends Microbiol._ 8, 478–480 (2000). Article  CAS  PubMed  Google Scholar  * Swanson, M. S. & Hammer, B. K. _Legionella pneumophila_

pathogenesis: a fateful journey from amoebae to macrophages. _Annu. Rev. Microbiol._ 54, 567–613 (2000). Article  CAS  PubMed  Google Scholar  * McLendon, M. K., Apicella, M. A. & Allen,

L. A. _Francisella tularensis_: taxonomy, genetics, and immunopathogenesis of a potential agent of biowarfare. _Annu. Rev. Microbiol._ 60, 167–185 (2006). Article  CAS  PubMed  PubMed

Central  Google Scholar  * Santic, M., Molmeret, M., Klose, K. E. & Abu, K. Y. _Francisella tularensis_ travels a novel, twisted road within macrophages. _Trends Microbiol._ 14, 37–44

(2006). Article  CAS  PubMed  Google Scholar  * Sjostedt, A. Intracellular survival mechanisms of _Francisella tularensis_, a stealth pathogen. _Microbes Infect._ 8, 561–567 (2006). Article

  PubMed  CAS  Google Scholar  * Vogel, J. P. & Isberg, R. R. Cell biology of _Legionella pneumophila_. _Curr. Opin. Microbiol._ 2, 30–34 (1999). Article  CAS  PubMed  Google Scholar  *

Roy, C. R. & Tilney, L. G. The road less traveled: transport of _Legionella_ to the endoplasmic reticulum. _J. Cell Biol._ 158, 415–419 (2002). Article  CAS  PubMed  PubMed Central 

Google Scholar  * Prentice, M. B. & Rahalison, L. Plague. _Lancet_ 369, 1196–1207 (2007). Article  PubMed  Google Scholar  * Wren, B. W. The yersiniae — a model genus to study the rapid

evolution of bacterial pathogens. _Nature Rev. Microbiol._ 1, 55–64 (2003). Article  CAS  Google Scholar  * Zhou, D., Han, Y. & Yang, R. Molecular and physiological insights into plague

transmission, virulence and etiology. _Microbes Infect._ 8, 273–284 (2006). Article  CAS  PubMed  Google Scholar  * Pujol, C. & Bliska, J. B. The ability to replicate in macrophages is

conserved between _Yersinia pestis_ and _Yersinia pseudotuberculosis_. _Infect. Immun._ 71, 5892–5899 (2003). Article  CAS  PubMed  PubMed Central  Google Scholar  * Tauxe, R. V. Salad and

pseudoappendicitis: _Yersinia pseudotuberculosis_ as a foodborne pathogen. _J. Infect. Dis._ 189, 761–763 (2004). Article  PubMed  Google Scholar  * Fukushima, H. Direct isolation of

_Yersinia pseudotuberculosis_ from fresh water in Japan. _Appl. Environ. Microbiol._ 58, 2688–2690 (1992). Article  CAS  PubMed  PubMed Central  Google Scholar  * Eisen, R. J. et al.

Persistence of _Yersinia pestis_ in soil under natural conditions. _Emerg. Infect. Dis._ 14, 941–943 (2008). Article  PubMed  PubMed Central  Google Scholar  * Drancourt, M., Houhamdi, L.

& Raoult, D. _Yersinia pestis_ as a telluric, human ectoparasite-borne organism. _Lancet Infect. Dis._ 6, 234–241 (2006). Article  PubMed  Google Scholar  * Cavanaugh, D. C. &

Randall, R. The role of multiplication of _Pasteurella pestis_ in mononuclear phagocytes in the pathogenesis of flea-borne plague. _J. Immunol._ 83, 348–363 (1959). CAS  PubMed  Google

Scholar  * Bacon, G. A. & Burrows, T. W. The basis of virulence in _Pasteurella pestis_: an antigen determining virulence. _Br. J. Exp. Pathol._ 37, 481–493 (1956). CAS  PubMed  PubMed

Central  Google Scholar  * Pujol, C. & Bliska, J. B. Turning _Yersinia_ pathogenesis outside in: subversion of macrophage function by intracellular yersiniae. _Clin. Immunol._ 114,

216–226 (2005). Article  CAS  PubMed  Google Scholar  * Lathem, W. W., Crosby, S. D., Miller, V. L. & Goldman, W. E. Progression of primary pneumonic plague: a mouse model of infection,

pathology, and bacterial transcriptional activity. _Proc. Natl Acad. Sci. USA_ 102, 17786–17791 (2005). Article  CAS  PubMed  PubMed Central  Google Scholar  * Viboud, G. I. & Bliska, J.

B. _Yersinia_ outer proteins: role in modulation of host cell signaling responses and pathogenesis. _Annu. Rev. Microbiol._ 59, 69–89 (2005). Article  CAS  PubMed  Google Scholar  *

Marketon, M. M., DePaolo, R. W., DeBord, K. L., Jabri, B. & Schneewind, O. Plague bacteria target immune cells during infection. _Science_ 309, 1739–1741 (2005). Article  CAS  PubMed 

PubMed Central  Google Scholar  * Du, Y., Rosqvist, R. & Forsberg, A. Role of fraction 1 antigen of _Yersinia pestis_ in inhibition of phagocytosis. _Infect. Immun._ 70, 1453–1460

(2002). Article  CAS  PubMed  PubMed Central  Google Scholar  * Finegold, M. J. Pneumonic plague in monkeys. An electron microscopic study. _Am. J. Pathol._ 54, 167–185 (1969). CAS  PubMed 

PubMed Central  Google Scholar  * Meyer, K. F. Immunity in plague; a critical consideration of some recent studies. _J. Immunol._ 64, 139–163 (1950). CAS  PubMed  Google Scholar  * Bosio, C.

M., Goodyear, A. W. & Dow, S. W. Early interaction of _Yersinia pestis_ with APCs in the lung. _J. Immunol._ 175, 6750–6756 (2005). Article  CAS  PubMed  Google Scholar  * Bubeck, S.

S., Cantwell, A. M. & Dube, P. H. Delayed inflammatory response to primary pneumonic plague occurs in both outbred and inbred mice. _Infect. Immun._ 75, 697–705 (2007). Article  CAS 

PubMed  Google Scholar  * Groisman, E. A. The pleiotropic two-component regulatory system PhoP–PhoQ. _J. Bacteriol._ 183, 1835–1842 (2001). Article  CAS  PubMed  PubMed Central  Google

Scholar  * Ernst, R. K., Guina, T. & Miller, S. I. How intracellular bacteria survive: surface modifications that promote resistance to host innate immune responses. _J. Infect. Dis._

179 (Suppl. 2), 326–330 (1999). Article  Google Scholar  * Oyston, P. C. et al. The response regulator PhoP is important for survival under conditions of macrophage-induced stress and

virulence in _Yersinia pestis_. _Infect. Immun._ 68, 3419–3425 (2000). Article  CAS  PubMed  PubMed Central  Google Scholar  * Grabenstein, J. P., Fukuto, H. S., Palmer, L. E. & Bliska,

J. B. Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of _Yersinia pestis_ in macrophages. _Infect. Immun._ 74, 3727–3741 (2006).

Article  CAS  PubMed  PubMed Central  Google Scholar  * Sebbane, F., Gardner, D., Long, D., Gowen, B. B. & Hinnebusch, B. J. Kinetics of disease progression and host response in a rat

model of bubonic plague. _Am. J. Pathol._ 166, 1427–1439 (2005). Article  PubMed  PubMed Central  Google Scholar  * Sebbane, F., Jarrett, C. O., Gardner, D., Long, D. & Hinnebusch, B. J.

Role of the _Yersinia pestis_ plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague. _Proc. Natl Acad. Sci. USA_ 103, 5526–5530 (2006).

Article  CAS  PubMed  PubMed Central  Google Scholar  * Jarrett, C. O. et al. Transmission of _Yersinia pestis_ from an infectious biofilm in the flea vector. _J. Infect. Dis._ 190, 783–792

(2004). Article  PubMed  Google Scholar  * Hinnebusch, B. J. The evolution of flea-borne transmission in _Yersinia pestis_. _Curr. Issues Mol. Biol._ 7, 197–212 (2005). CAS  PubMed  Google

Scholar  * Lukaszewski, R. A. et al. Pathogenesis of _Yersinia pestis_ infection in BALB/c mice: effects on host macrophages and neutrophils. _Infect. Immun._ 73, 7142–7150 (2005). Article 

CAS  PubMed  PubMed Central  Google Scholar  * Diamond, R. D. & Bennett, J. E. Growth of _Cryptococcus neoformans_ within human macrophages _in vitro_. _Infect. Immun._ 7, 231–236

(1973). Article  CAS  PubMed  PubMed Central  Google Scholar  * Casadevall, A. & Perfect, J. R. _Cryptococcus neoformans_ (American Society for Microbiology, Washington DC, 1998). Book 

Google Scholar  * Feldmesser, M., Tucker, S. C. & Casadevall, A. Intracellular parasitism of macrophages by _Cryptococcus neoformans_. _Trends Microbiol._ 9, 273–278 (2001). Article  CAS

  PubMed  Google Scholar  * Rittershaus, P. C. et al. Glucosylceramide synthase is an essential regulator of pathogenicity of _Cryptococcus neoformans_. _J. Clin. Invest._ 116, 1651–1659

(2006). Article  CAS  PubMed  PubMed Central  Google Scholar  * Weeks, S., Hill, J., Friedlander, A. & Welkos, S. Anti-V antigen antibody protects macrophages from _Yersinia

pestis_-induced cell death and promotes phagocytosis. _Microb. Pathog._ 32, 227–237 (2002). Article  CAS  PubMed  Google Scholar  * Cowan, C., Philipovskiy, A. V., Wulff-Strobel, C. R., Ye,

Z. & Straley, S. C. Anti-LcrV antibody inhibits delivery of Yops by _Yersinia pestis_ KIM5 by directly promoting phagocytosis. _Infect. Immun._ 73, 6127–6137 (2005). Article  CAS  PubMed

  PubMed Central  Google Scholar  * Lahteenmaki, K., Kuusela, P. & Korhonen, T. K. Bacterial plasminogen activators and receptors. _FEMS Microbiol. Rev._ 25, 531–552 (2001). Article  CAS

  PubMed  Google Scholar  * Cowan, C., Jones, H. A., Kaya, Y. H., Perry, R. D. & Straley, S. C. Invasion of epithelial cells by _Yersinia pestis_: evidence for a _Y. pestis_-specific

invasin. _Infect. Immun._ 68, 4523–4530 (2000). Article  CAS  PubMed  PubMed Central  Google Scholar  * Liu, F., Chen, H., Galvan, E. M., Lasaro, M. A. & Schifferli, D. M. Effects of Psa

and F1 on the adhesive and invasive interactions of _Yersinia pestis_ with human respiratory tract epithelial cells. _Infect. Immun._ 74, 5636–5644 (2006). Article  CAS  PubMed  PubMed

Central  Google Scholar  * Chang, Y. C. et al. Cryptococcal yeast cells invade the central nervous system via transcellular penetration of the blood–brain barrier. _Infect. Immun._ 72,

4985–4995 (2004). Article  CAS  PubMed  PubMed Central  Google Scholar  * Chen, S. H. et al. _Cryptococcus neoformans_ induces alterations in the cytoskeleton of human brain microvascular

endothelial cells. _J. Med. Microbiol._ 52, 961–970 (2003). Article  CAS  PubMed  Google Scholar  * Shao, X. et al. An innate immune system cell is a major determinant of species-related

susceptibility differences to fungal pneumonia. _J. Immunol._ 175, 3244–3251 (2005). Article  CAS  PubMed  Google Scholar  * Feldmesser, M., Kress, Y., Novikoff, P. & Casadevall, A.

_Cryptococcus neoformans_ is a facultative intracellular pathogen in murine pulmonary infection. _Infect. Immun._ 68, 4225–4237 (2000). Article  CAS  PubMed  PubMed Central  Google Scholar 

* Zaragoza, O., Alvarez, M., Telzak, A., Rivera, J. & Casadevall, A. The relative susceptibility of mouse strains to pulmonary _Cryptococcus neoformans_ infection is associated with

pleiotropic differences in the immune response. _Infect. Immun._ 75, 2729–2739 (2007). Article  CAS  PubMed  PubMed Central  Google Scholar  * Straley, S. C. & Harmon, P. A. _Yersinia

pestis_ grows within phagolysosomes in mouse peritoneal macrophages. _Infect. Immun._ 45, 655–659 (1984). Article  CAS  PubMed  PubMed Central  Google Scholar  * Tucker, S. C. &

Casadevall, A. Replication of _Cryptococcus neoformans_ in macrophages is accompanied by phagosomal permeabilization and accumulation of vesicles containing polysaccharide in the cytoplasm.

_Proc. Natl Acad. Sci. USA_ 99, 3165–3170 (2002). Article  CAS  PubMed  PubMed Central  Google Scholar  * Levitz, S. M. et al. _Cryptococcus neoformans_ resides in an acidic phagolysosome of

human macrophages. _Infect. Immun._ 67, 885–890 (1999). Article  CAS  PubMed  PubMed Central  Google Scholar  * Tsukano, H. et al. _Yersinia pseudotuberculosis_ blocks the phagosomal

acidification of B10.A mouse macrophages through the inhibition of vacuolar H+-ATPase activity. _Microb. Pathog._ 27, 253–263 (1999). Article  CAS  PubMed  Google Scholar  * Vieira, O. V.,

Botelho, R. J. & Grinstein, S. Phagosome maturation: aging gracefully. _Biochem. J._ 366, 689–704 (2002). Article  CAS  PubMed  PubMed Central  Google Scholar  * Cox, G. M. et al.

Extracellular phospholipase activity is a virulence factor for _Cryptococcus neoformans_. _Mol. Microbiol._ 39, 166–175 (2001). Article  CAS  PubMed  Google Scholar  * Levitz, S. M.,

Harrison, T. S., Tabuni, A. & Liu, X. Chloroquine induces human nononuclear phagocytes to inhibit and kill _Cryptococcus neoformans_ by a mechanism independent of iron deprivation. _J.

Clin. Invest._ 100, 1640–1646 (1997). Article  CAS  PubMed  PubMed Central  Google Scholar  * Harrison, T. S., Griffin, G. E. & Levitz, S. M. Conditional lethality of the diprotic weak

bases chloroquine and quinacrine against _Cryptococcus neoformans_. _J. Infect. Dis._ 182, 283–289 (2000). Article  CAS  PubMed  Google Scholar  * Perry, R. D. & Fetherston, J. D.

_Yersinia pestis_ — etiologic agent of plague. _Clin. Microbiol. Rev._ 10, 35–66 (1997). Article  CAS  PubMed  PubMed Central  Google Scholar  * Perry, R. D., Mier, I. Jr & Fetherston,

J. D. Roles of the Yfe and Feo transporters of _Yersinia pestis_ in iron uptake and intracellular growth. _Biometals_ 20, 699–703 (2007). Article  CAS  PubMed  Google Scholar  * Pujol, C.,

Grabenstein, J. P., Perry, R. D. & Bliska, J. B. Replication of _Yersinia pestis_ in interferon γ-activated macrophages requires _ripA_, a gene encoded in the pigmentation locus. _Proc.

Natl Acad. Sci. USA_ 102, 12909–12914 (2005). Article  CAS  PubMed  PubMed Central  Google Scholar  * Goulding, C. W. et al. The structure and computational analysis of _Mycobacterium

tuberculosis_ protein CitE suggest a novel enzymatic function. _J. Mol. Biol._ 365, 275–283 (2007). Article  CAS  PubMed  Google Scholar  * Brown, S. M., Campbell, L. T. & Lodge, J. K.

_Cryptococcus neoformans_, a fungus under stress. _Curr. Opin. Microbiol._ 10, 320–325 (2007). Article  CAS  PubMed  PubMed Central  Google Scholar  * Giles, S. S. et al. The _Cryptococcus

neoformans_ catalase gene family and its role in antioxidant defense. _Eukaryot. Cell_ 5, 1447–1459 (2006). Article  CAS  PubMed  PubMed Central  Google Scholar  * de Jesus-Berrios, M. et

al. Enzymes that counteract nitrosative stress promote fungal virulence. _Curr. Biol._ 13, 1963–1968 (2003). Article  CAS  PubMed  Google Scholar  * Missall, T. A. & Lodge, J. K.

Function of the thioredoxin proteins in _Cryptococcus neoformans_ during stress or virulence and regulation by putative transcriptional modulators. _Mol. Microbiol._ 57, 847–858 (2005).

Article  CAS  PubMed  Google Scholar  * Narasipura, S. D., Chaturvedi, V. & Chaturvedi, S. Characterization of _Cryptococcus neoformans_ variety gattii SOD2 reveals distinct roles of the

two superoxide dismutases in fungal biology and virulence. _Mol. Microbiol._ 55, 1782–1800 (2005). Article  CAS  PubMed  Google Scholar  * Giles, S. S., Batinic-Haberle, I., Perfect, J. R.

& Cox, G. M. _Cryptococcus neoformans_ mitochondrial superoxide dismutase: an essential link between antioxidant function and high-temperature growth. _Eukaryot. Cell_ 4, 46–54 (2005).

Article  CAS  PubMed  PubMed Central  Google Scholar  * Cox, G. M. et al. Superoxide dismutase influences the virulence of _Cryptococcus neoformans_ by affecting growth within macrophages.

_Infect. Immun._ 71, 173–180 (2003). Article  CAS  PubMed  PubMed Central  Google Scholar  * Chatuverdi, V., Wong, B. & Newman, S. L. Oxidative killing of _Cryptococcus neoformans_ by

human leukocytes. Evidence that fungal mannitol protects by scavenging reactive oxygen intermediates. _J. Immunol._ 156, 3836–3840 (1996). Google Scholar  * Shea, J. M., Kechichian, T. B.,

Luberto, C. & Del Poeta, M. The cryptococcal enzyme inositol phosphosphingolipid-phospholipase C confers resistance to the antifungal effects of macrophages and promotes fungal

dissemination to the central nervous system. _Infect. Immun._ 74, 5977–5988 (2006). Article  CAS  PubMed  PubMed Central  Google Scholar  * Rodrigues, M. L. et al. Vesicular polysaccharide

export in _Cryptococcus neoformans_ is a eukaryotic solution to the problem of fungal trans-cell wall transport. _Eukaryot. Cell_ 6, 48–59 (2007). Article  CAS  PubMed  Google Scholar  *

Rodrigues, M. L. et al. Extracellular vesicles produced by _Cryptococcus neoformans_ contain protein components associated with virulence. _Eukaryot. Cell_ 7, 58–67 (2008). Article  CAS 

PubMed  Google Scholar  * Beatty, W. L. et al. Trafficking and release of mycobacterial lipids from infected macrophages. _Traffic_ 1, 235–247 (2000). Article  CAS  PubMed  Google Scholar  *

Ma, H., Croudace, J. E., Lammas, D. A. & May, R. C. Direct cell-to-cell spread of a pathogenic yeast. _BMC Immunol._ 8, 15 (2007). Article  PubMed  PubMed Central  CAS  Google Scholar 

* Alvarez, M. & Casadevall, A. Cell-to-cell spread and massive vacuole formation after _Cryptococcus neoformans_ infection of murine macrophages. _BMC Immunol._ 8, 16 (2007). Article 

PubMed  PubMed Central  CAS  Google Scholar  * Greub, G. & Raoult, D. Microorganisms resistant to free-living amoebae. _Clin. Microbiol. Rev._ 17, 413–433 (2004). Article  PubMed  PubMed

Central  Google Scholar  * Steenbergen, J. N., Nosanchuk, J. D., Malliaris, S. D. & Casadevall, A. Interaction of _Blastomyces dermatitidis_, _Sporothrix schenckii_, and _Histoplasma

capsulatum_ with _Acanthamoeba castellanii_. _Infect. Immun._ 72, 3478–3488 (2004). Article  CAS  PubMed  PubMed Central  Google Scholar  * Alvarez, M. & Casadevall, A. Phagosome fusion

and extrusion, and host cell survival following _Cryptococcus neoformans_ phagocytosis by macrophages. _Curr. Biol._ 16, 2161–2165 (2006). Article  CAS  PubMed  Google Scholar  * Newman, S.

L. Macrophages in host defense against _Histoplasma capsulatum_. _Trends Microbiol._ 7, 67–71 (1999). Article  CAS  PubMed  Google Scholar  * Woods, J. P. Knocking on the right door and

making a comfortable home: _Histoplasma capsulatum_ intracellular pathogenesis. _Curr. Opin. Microbiol._ 6, 327–331 (2003). Article  CAS  PubMed  Google Scholar  * Marion, C. L., Rappleye,

C. A., Engle, J. T. & Goldman, W. E. An α-(1,4)-amylase is essential for α-(1,3)-glucan production and virulence in _Histoplasma capsulatum_. _Mol. Microbiol._ 62, 970–983 (2006).

Article  CAS  PubMed  Google Scholar  Download references ACKNOWLEDGEMENTS Work in the laboratory of J.B.B. on intracellular replication of _Y. pestis_ in macrophages is supported by Public

Health Service (PHS) grant AI055621. Work in the laboratory of A.C. on intracellular pathogenesis of _C. neoformans_ is supported by PHS grant HL59842-11. A.C. and J.B.B. both contribute

research to, and receive support from, the Northeastern Biodefense Center (grant number 5U54AI057158-05). The authors thank C. Pujol and M. Alvarez for providing the electron-microscopy

images used in the figures and for reviewing the manuscript. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * James B. Bliska is at the Department of Molecular Genetics and Microbiology and

Center for Infectious Diseases, School of Medicine, Stony Brook University, Stony Brook, New York, 11794 New York, USA., James B. Bliska * Arturo Casadevall is at the Departments of

Microbiology & Immunology and the Division of Infectious Diseases of the Department of Medicine, Albert Einstein College of Medicine, Bronx, New York, 10461 New York, USA., Arturo

Casadevall Authors * James B. Bliska View author publications You can also search for this author inPubMed Google Scholar * Arturo Casadevall View author publications You can also search for

this author inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to Arturo Casadevall. RELATED LINKS RELATED LINKS DATABASES ENTREZ GENOME PROJECT _Cryptococcus neoformans_

_Francisella tularensis_ _Histoplasma capsulatu m_ _Legionella pneumophila_ _Mycobacterium tuberculosis_ _S. Typhimurium_ _Toxoplasma gondii_ _Yersinia pestis_ _Yersinia pseudotuberculosis_

FURTHER INFORMATION James B. Bliska's homepage Arturo Casadevall's homepage RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Bliska, J.,

Casadevall, A. Intracellular pathogenic bacteria and fungi — a case of convergent evolution?. _Nat Rev Microbiol_ 7, 165–171 (2009). https://doi.org/10.1038/nrmicro2049 Download citation *

Published: 22 December 2008 * Issue Date: February 2009 * DOI: https://doi.org/10.1038/nrmicro2049 SHARE THIS ARTICLE Anyone you share the following link with will be able to read this

content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing initiative