Bacterial α2-macroglobulins: colonization factors acquired by horizontal gene transfer from the metazoan genome?

Budd Aidan, Blandin Stephanie, Levashina, Gibson

Description

Invasive bacteria are known to have captured and adapted eukaryotic host genes. They also readily acquire colonizing genes from other bacteria by horizontal gene transfer. Closely related species such as Helicobacter pylori and Helicobacter hepaticus , which exploit different host tissues, share almost none of their colonization genes. The protease inhibitor α 2 -macroglobulin provides a major metazoan defense against invasive bacteria, trapping attacking proteases required by parasites for successful invasion. Results Database searches with metazoan α 2 -macroglobulin sequences revealed homologous sequences in bacterial proteomes. The bacterial α 2 -macroglobulin phylogenetic distribution is patchy and violates the vertical descent model. Bacterial α 2 -macroglobulin genes are found in diverse clades, including purple bacteria (proteobacteria), fusobacteria, spirochetes, bacteroidetes, deinococcids, cyanobacteria, planctomycetes and thermotogae. Most bacterial species with bacterial α 2 -macroglobulin genes exploit higher eukaryotes (multicellular plants and animals) as hosts. Both pathogenically invasive and saprophytically colonizing species possess bacterial α 2 -macroglobulins, indicating that bacterial α 2 -macroglobulin is a colonization rather than a virulence factor. Conclusions Metazoan α 2 -macroglobulins inhibit proteases of pathogens. The bacterial homologs may function in reverse to block host antimicrobial defenses. α 2 -macroglobulin was probably acquired one or more times from metazoan hosts and has then spread widely through other colonizing bacterial species by more than 10 independent horizontal gene transfers. yfhM -like bacterial α 2 -macroglobulin genes are often found tightly linked with pbpC , encoding an atypical peptidoglycan transglycosylase, PBP1C, that does not function in vegetative peptidoglycan synthesis. We suggest that YfhM and PBP1C are coupled together as a periplasmic defense and repair system. Bacterial α 2 -macroglobulins might provide useful targets for enhancing vaccine efficacy in combating infections.

Informations

• Publié par: biomed
• Publié le: 01 janvier 2004
• Nombre de lectures: 16
• Langue: English

Extrait

2eBV R t0u oal e 0dlu.4d s m e e a 5 r , c Is h sue 6, Article R38 Open Access Bacterial α 2 -macroglobulins: colonizat ion factors acquired by horizontal gene transfer from the metazoan genome? Aidan Budd * , Stephanie Blandin * , Elena A Levashina  and Toby J Gibson * Addresses: * European Molecular Biology Laboratory, 69012 Heidelberg, Germany.  UPR 9022 du CNRS, IBMC, rue René Descartes, F-67087 Strasbourg CEDEX, France. Correspondence: Toby J Gibson. E-mail: [e-mail]

Published: 26 May 2004 Received: 20 February 2004 Genome Biology 2004, 5: R38 Revised: 2 April 2004 Accepted: 8 April 2004 The electronic version of this arti cle is the complete one and can be found online at http://genomebiology.com/2004/5/6/R38 © 2004 Budd et al .; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitt ed in all media for any purpose, provided this notice is pr eserved along with the article's original URL. p wB<br a >pho c i> t vcIi e hdn r   i e vaxs a  l  sbpai α l yvo 2  mei-h tao mbjdr a o i c frzft ro e mon r git e l a tno l a t b zgrhou e ol aniks n et   s t do:ri eswcafseo n ul nstoefsosene ,ri   h.zs a  hgCvt a liei o r n cse sae atlfpl yiat mncurtevr o le a srt s dt   i env a doenc   nsqdb pe a u eicodrctfai e etrdpshi t a e bs,iy durt    rhe c hau o  plrkaiopaszi nron<iyznigo t at a >tiitlc Hot gahn e c olignksc e it   o n tgbg e r a snpc.n retTo s ef.trh  e Trp   ahfypsl r e y o s r tmaire le s<atqsoh/u e irt   iier>nmeaah d en i tl b da i y z t <a o picatra qn>r α uaHgi<sr e sitlnu iecocbs o  m>flb o 2ear?n< cist/zuesircnu cgbhe e>gs-epsfnamuteial s c i frunr o svg<alms/o i  tb o t>unh,l. i<enr/  

Abstract Background: Invasive bacteria are known to have capt ured and adapted eukaryotic host genes. They also readily acquire colonizing genes from other bacteria by horizontal gene transfer. Closely related species such as Helicobacter pylori and Helicobacter hepaticus , which exploit different host tissues, share almost none of their colonization gene s. The protease inhibitor α 2 -macroglobulin provides a major metazoan defense against invasive bacteria, trapping attacking proteases required by parasites for successful invasion. Results: Database searches with metazoan α 2 -macroglobulin sequences revealed homologous sequences in bacterial proteomes. The bacterial α 2 -macroglobulin phyloge netic distribution is patchy and violates the vertic al descent model. Bacterial α 2 -macroglobulin genes are found in diverse clades, including purple ba cteria (proteobacteria), fusobacteri a, spirochetes, bacteroidetes, deinococcids, cyanobacteria, pl anctomycetes and thermotogae. Most bacterial species with bacterial α 2 -macroglobulin genes exploit higher eukaryot es (multicellular plants and animals) as hosts. Both pathogenically inva sive and saprophytically colonizing species possess bacterial α 2 - macroglobulins, indicating that bacterial α 2 -macroglobulin is a colonization rather than a virulence factor. Conclusions: Metazoan α 2 -macroglobulins inhibit protease s of pathogens. The bacterial homologs may function in reverse to block host antimicrobial defenses. α 2 -macroglobulin was probably acquired one or more times from metazo an hosts and has then spread widely through other colonizing bacterial specie s by more than 10 independen t horizontal gene transfers. yfhM -like bacterial α 2 -macroglobulin genes are often found tightly linked with pbpC , encoding an atypical peptidoglycan transglycosylase, PBP1C, that do es not function in vegetative peptidoglycan synthesis. We suggest that YfhM and PBP1C are coupled together as a periplasmic defense and repair system. Bacterial α 2 -macroglobulins might provide usef ul targets for enhancing vaccine efficacy in combating infections.

Genome Biology 2004, 5: R38