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Proteins of Generalist and Specialist Pathogens Differ in Their Amino Acid Composition

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Proteins of Generalist and Specialist Pathogens Differ in Their Amino Acid Composition Published Online: 17 July, 2018 | Supp Info: http://doi.org/10.26508/lsa.201800017 Downloaded from life-science-alliance.org on 23 September, 2021 Research Article Proteins of generalist and specialist pathogens differ in their amino acid composition Luz P Blanco1,* , Bryan L Payne2, Felix Feyertag2, David Alvarez-Ponce2 Pathogens differ in their host specificities, with species infecting by the early genetic code, and which were spontaneously generated a unique host (specialist pathogens) and others having a wide in Miller’s spark discharge experiments [Doi et al, 2005; Parker host range (generalists). Molecular determinants of pathogen’s et al, 2011]) have been associated with proteins with enhanced host range remain poorly understood. Secreted proteins of promiscuity and solubility. In contrast, non-primitive amino generalist pathogens are expected to have a broader range of acids have been correlated with lower solubility, enhanced ri- intermolecular interactions (i.e., higher promiscuity) compared gidity, and highly structured conformations (Davidson et al, 1995; with their specialist counterparts. We hypothesize that this in- James & Tawfik, 2003; Doi et al, 2005). Thus, we hypothesize that, creased promiscuity of generalist secretomes may be based on an for an organism to be highly promiscuous or capable of elevated content of primitive amino acids and intrinsically dis- infecting/interacting with multiple hosts, their secreted and ordered regions, as these features are known to increase protein membrane proteins should be enriched in primitive amino acids flexibility and interactivity. Here, we measure the proportion of compared with secreted and membrane proteins of host- primitive amino acids and percentage of intrinsically disordered restricted specialist pathogens. Primitive amino acids in sur- residues in secreted, membrane, and cytoplasmic proteins from face exposed proteins might aid generalists’ ability to interact pathogens with different host specificity. Supporting our pre- with a broader range of proteins from different hosts. On the diction, there is a significant general enrichment for primitive contrary, surface-exposed proteins from specialists do not re- amino acids and intrinsically disordered regions in proteins from quire to interact with a high repertoire of proteins because they generalists compared to specialists, particularly among secreted are host-restricted, and thus, they might have a reduced amount proteins in prokaryotes. Our findings support our hypothesis that of primitive amino acids. secreted proteins’ amino acid composition and disordered In addition, the protein’s ability to establish intermolecular content influence the pathogens’ host range. interactions is also dictated by their content of intrinsically dis- ordered regions (Tompa et al, 2015; Ahrens et al, 2017). Intrinsically DOI 10.26508/lsa.201800017 | Received 5 January 2018 | Revised 9 July disordered regions are protein domains that lack a stable structural 2018 | Accepted 10 July 2018 | Published online 17 July 2018 conformation and whose structure oscillates among different al- ternative conformations. Such regions confer flexibility to the proteins, facilitating their interactions with other molecules. In- Introduction deed, intrinsically disordered proteins (those with a high content of intrinsically disordered regions) tend to be highly connected Certain pathogens are highly species-specific, whereas others affect (Dyson & Wright, 2002; Dunker et al, 2005). Thus, it is possible that a broad range of hosts. However, the molecular bases of host range the secreted proteins of the secreted and membrane proteins of variability remain poorly understood (Pan et al, 2014). Secreted and generalist pathogens are highly disordered compared with those of membrane proteins are known to play important roles in host– specialists. pathogen interactions, and thus their interaction capabilities are Here, we compare the frequency of primitive amino acid residues expected to play a key role in determining host range, with generalist and the percentage of disordered regions of proteins from several secreted and membrane proteins being capable of interacting with pairs of generalists and specialists. In agreement with our predic- a wider range of molecules than their specialist counterparts. tions, we observe increased amounts of primitive amino acids and Primitive amino acids (those believed to have predominated disordered regions predominantly in secreted proteins from gen- under prebiotic conditions, found in meteorite analysis, produced eralists compared with specialist pathogens. 1Systemic Autoimmunity Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, MD, USA 2Department of Biology, University of Nevada, Reno, NV, USA Correspondence: [email protected]; [email protected] *Luz P Blanco contributed to this work in her personal capacity. The views expressed are her own and do not necessarily represent the view of the National Institutes of Health or the US Government. Felix Feyertag’s present address is Structural Genomics Consortium; Target Discovery Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK ©2018Blanco et al. https://doi.org/10.26508/lsa.201800017 vol 1 | no 4 | e201800017 1of7 Table 1. Pathogens with their respective host range used in this study. Host range Niche of infection Type of pathogen Reference or source Specialist/host adapted Generalist (species) L. longbeachae (Homo Facultative intracellular, lung Bacteria, Gram (Marra & Shuman, 1992; Whiley & L. pneumophila sapiens) environment negative Bentham, 2011)a S. enterica Typhi (H. S. enterica Bacteria, Gram Facultative intracellular, systemic (Sabbagh et al, 2010)a sapiens) Typhimurium negative Bacteria, Gram V. cholerae O1 (H. sapiens) V. vulnificus Extracellular, mucosal pathogen (Jones & Oliver, 2009; Safa et al, 2010)a negative Intracellular, systemic and lung Bacteria, (Mikota & Maslow, 2011; Legendre et al, M. leprae (H. sapiens) M. bovis environment actinobacteria 2012)a Facultative intracellular, vector Bacteria, Gram (Chomel et al, 2004; Veracx & Raoult, B. quintana (H. sapiens) B. henselae transmissible, systemic negative 2012)a Vector transmissible/extracellular, Bacteria, spirochete B. recurrentis (H. sapiens) B. burgdorferi (Veracx & Raoult, 2012)a,b systemic Systemic Obligate intracellular, lung environment/ C. pneumonia (H. sapiens) C. trachomatis Bacteria (Beare et al, 2011)a sexually transmissible, eye infections Bacteria, Gram R. prowazekii (H. sapiens) R. rickettsii Obligate intracellular, systemic (Beare et al, 2011)a negative C. rodentium (Mus Bacteria, Gram C. freundii Extracellular, mucosal pathogen (Borenshtein et al, 2008; Bai et al, 2012)a,c musculus) negative S. enterica Gallinarum S. enterica Facultative intracellular, systemic/ Bacteria, Gram (Braden, 2006; Blondel et al, 2013)d (Gallus gallus) Enteritidis mucosal environment negative Streptococcus pyogenes Bacteria, Gram (Cunningham, 2000; Abdelsalam et al, S. dysgalactiae Extracellular (H. sapiens) positive 2013)a Bacillus cereus (human Bacteria, Gram B. anthracis Extracellular/obligate intracellular (Kotiranta et al, 2000; Spencer, 2003)a opportunistic) positive M. intracellulare (H. Intracellular, and systemic and lung Bacteria, M. avium (Claeys & Robinson, 2018)a sapiens) environment actinobacteria C. albicans (H. sapiens) C. glabrata Extracellular Fungus (Brunke & Hube, 2013; Mayer et al, 2013)e Vector transmissible/extracellular and P. falciparum (H. sapiens) B. microti Unicellular protozoa (Gray et al, 2010; Prugnolle et al, 2011) intracellular Vector transmissible/egg consumption/ (Woolhouse et al, 2001; Nejsum et al, W. bancrofti (H. sapiens) A. suum Nematode extracellular 2012) ahttps://my.absa.org/tiki-index.php?page=Riskgroups. bhttp://www.phac-aspc.gc.ca/lab-bio/res/psds-ftss/msds21e-eng.php. chttps://www.msdsonline.com/resources/msds-resources/free-safety-data-sheet-index/citrobacter-spp/. dhttp://www.sanger.ac.uk/resources/downloads/bacteria/salmonella.html. ehttp://www.phac-aspc.gc.ca/lab-bio/res/psds-ftss/msds30e-eng.php. Results and in their niches of infection. For comparison, broad generalists of the same species, the same genus, or closely related lineages, The proteomes of 16 pairs of closely related pathogens, with each were chosen (Table 1). Eukaryote human-adapted pathogens in- pair containing one generalist and one species-specific pathogen, cluded in our analyses were the fungus Candida albicans (Mayer were compared in this work (Table 1). These included 13 pairs of et al, 2013), the unicellular protozoon Plasmodium falciparum bacteria and 3 pairs of eukaryotes. Our list includes traditional (Woolhouse et al, 2001), and the nematode Wuchereria bancrofti human-specific bacterial pathogens such as Salmonella typhi (Woolhouse et al, 2001). For comparison, the fungus C. glabrata (Sabbagh et al, 2010), Vibrio cholerae (Safa et al, 2010), and My- (Brunke & Hube, 2013), the unicellular protozoon Babesia microti cobacterium leprae (Legendre et al, 2012), and other less well- (Gray et al, 2010), and the nematode Ascaris suum (Nejsum et al, characterized or recently emerged pathogens, such as Legionella 2012) were selected as broad host-range pathogens. longbeachae (Whiley & Bentham, 2011), Bartonella quintana (Veracx For each of the proteins of these organisms, we computed the & Raoult, 2012), and B. recurrentis (Veracx & Raoult, 2012). These ratio of primitive amino acids as AGVDE = [alanine
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