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There Ae Currently Three Fully Sequenced Deltaproteobacteria

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There Ae Currently Three Fully Sequenced Deltaproteobacteria עבודת גמר )תזה( לתואר Thesis for the degree דוקטור לפילוסופיה Doctor of Philosophy מוגשת למועצה המדעית של Submitted to the Scientific Council of the מכון ויצמן למדע Weizmann Institute of Science רחובות, ישראל Rehovot, Israel מאת By אופיר אבידן Ofir Avidan התגובה הראשונית של Bdellovibrio לטרף Early response of Bdellovibrio to its prey מנחים: :Advisors פרופסור שמואל פיטרוקובסקי )מכון Professor Shmuel Pietrokovski וויצמן( (WIS) פרופסור אדוארד יורקביץ Professor Edouard Jurkevitch )האוניברסיטה העברית בירושלים( The Hebrew University of) Jerusalem) חודש ושנה עבריים Month and Year שבט, תשע"ו January, 2016 Table of contents 1. List of abbreviations .................................................................................... 2 2. Abstract................................................................................................................ 3 4 ...................................................................................................................... תקציר .3 4. Introduction ...................................................................................................... 5 5. Research aims ................................................................................................ 12 6. Materials and methods ............................................................................ 13 7. Results ............................................................................................................... 18 7.1 Genetic manipulations in Bdellovibrio ................................................................. 18 7.2 Screen for attack phase genes ............................................................................. 23 7.2.1 Identification of attack phase core genes ................................................... 23 7.2.2 B. bacteriovorus HD100 genome encodes four different flp pili genes ...... 27 7.2.3 flp1, flp2 and flp4 are expressed during attack phase while flp3 is silent In all tested conditions ............................................................................... 30 7.2.4 flp1 and flp2 and flp4 do not mediate binding to biotic or abiotic surface ........................................................................................................ 33 7.2.5 The B. bacteriovorus HD100 and B. exovorus JSS TAD operons are Regulated by the flagellar sigma factor, fliA .............................................. 34 7.2.6 Attempts at identifying proteins interacting with bd0119 ......................... 36 7.3 BALO's TAD locus show increased diversity in environmental metagenomics 38 7.3.1 BALO contigs were identified from marine metagenome ......................... 38 7.3.2 Marine and non-marine Bdellovibrio differ in their TAD locus ................... 40 7.3.3 Searching for bd0108 orthologs ........................................................................ 42 7.4 Attempts at identifying Bdellovibrio host binding receptor ............................... 43 8. Discussion ........................................................................................................ 46 9. Appendix .......................................................................................................... 52 10. Bibliography .......................................................................................................... 58 1 1. List of abbreviations BALO: Bdellovibrio and like organisms B-ArHS: Bdellovibrio sp. ArSH B. ba-HD100: Bdellovibrio bacteriovorus HD100 B. ba-W: Bdellovibrio bacteriovorus W B. ex-JSS: Bdellovibrio exovorus JSS BSR: BLAST score ratio Bx- BAL6_X: Bacteriovorax sp. BAL6_X Bx- BSW11_IV: Bacteriovorax sp. BSW11_IV Bx-SEQ25_V: Bacteriovorax sp. Seq25_V DAP: diaminopimelic acid DNB: diluted Nutrient Broth E. coli: Escherichia coli Flp: fimbria-like protein HEPES: 4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid HYP: hypothetical protein H. ma-SJ: Halobacteriovorax marinus SJ PCR: polymerase chain reaction PYE: peptone yeast extract PWM: position weight matrix TAD: tight adherence 2 2. Abstract Bdellovibrio bacteriovorus is an obligate predator of bacteria that grows and divides within the periplasm of Gram-negative prey. To invade a bacterial prey cell, a free-swimming prey-searching attack phase (AP) Bdellovibrio cell attaches to a bacterial prey cell and alters its cell wall. Functions involved in these early steps of predation have been identified and characterized. This enables a greater understanding of the signaling process involved in predator-prey interactions. Nevertheless, early mediators necessary for prey invasion are still poorly detailed. Here, novel genes involved in essential early predation processes were identified and characterized. By analyzing genomic and transcriptomic data available for Bdellovibrio and like organisms (BALO's) which differ in predatory strategies and phylogeny, 43 genes expressed in B. bacteriovorus during early interactions with its prey were identified. Five of these genes cluster together in the tight adherence (TAD) operon, which encodes for two type IVb fimbriae-like proteins pili (flp1 and flp2) and the protein machinery for their processing and export. Two additional flp pilus-encoding genes (flp3 and flp4) were computationally identified at other locations along the chromosome. This defined the largest and most diverse type IVb complement known in a bacterium to date. Careful examination revealed that flp2 bears a different protein motif than other known flp proteins. Using genetic tools for deleting genes established in this work, it was demonstrated that deleting each of the expressed flp pili (flp1, flp2 and flp4) caused B. bacteriovorus to lose its predatory behavior without altering its adherence properties toward E. coli. By using conserved features of the TAD locus in the different BALO's I identified contigs with flp sequences from environmental metagenomic samples. Remarkably, the marine and non-marine environments each includes different flp sequence types and processing components. Furthermore, I identified Bd0108-like sequences that are associated with TAD operons. A common motif was found in non-marine Bd0108 orthologs. 3 It was further demonstrated that the B. bacteriovorus TAD operon, and therefore flp1 and flp2, is under regulation of the flagella sigma factor, FliA, while flp4 is not, and that, in contrast to other bacteria, fliA has become an essential gene in B. bacteriovorus. תקציר.3 Bdellovibrio bacteriovorus הינו חיידק טורף המתרבה וגדל בתוך פריפלסמה של חיידקים גרם שליליים אחרים. על מנת לפלוש לתא של הטרף הבקטריאלי, תא לא מתחלק של Bdellovibrio הנע במהירות ומחפש אחר טרף )attack phase, AP), נצמד לתא הטרף ומשנה את קיר התא. הפעילות הכלולה בשלבים מוקדמים אלו של הטריפה זוהתה ואופיינה, וממנה ניתן להבין את תהליך האיתות הכלול ביחסים בין הטורף לטרף. אף על פי כן, מתווכים מוקדמים/ראשוניים החיוניים לפלישה לטרף עדיין אינם מפורטים כיאות. במחקר זה זיהיתי ואפיינתי גנים חדשים הקשורים לשלבי הטריפה המוקדמים, באמצעות ניתוח נתונים גנומיים וטרנסקריפטומיים הזמינים עבור Bdellovibrio ואורגניזמים דומים )BALO's(, הנבדלים באסטרטגיות הטריפה ופילוגנזה. זיהיתי 43 גנים המתבטאים ב-B. bacteriovorus במהלך האינטרקציות הראשונות עם הטרף. חמישה מבין אותם גנים של B. bacteriovorus מקובצים יחדיו באופרון (Tight adherence (TAD , אופרון זה מקודד ל 2 חלבוני פילי מסוג flp1( flp ו flp2( השייכים לקבוצה גדולה יותר של פילי מסוג 4b. כמו כן באופרון ה TAD מקודדים חלבונים האחראים על עיבוד והצגה של ה- flp על גבי קרום התא. כמו כן זיהיתי באמצעיים חישוביים שני חלבונים נוספים מסוג flp3( flp ו flp4( באתרים אחרים בכרומוזום. גיליתי באנליזה ביואינפורמטית נוספת כי flp2 מקודד למוטיב שונה מזה של flp אחרים. במהלך עבודה זו מצאתי כי רק flp2 ,flp1 וflp4- מבוטאים ועל כן מחיקה של גנים אלה גרמה ל Bdellovibrio לאבד את יכולת הטריפה מבלי לפגוע ביכולתו להצמד לתאי הטרף. בעזרת שימוש במאפיינים שמורים של אופרון ה TAD, הצלחתי לזהות מקטעי DNA של BALO's ממאגרים מטאגנומיים, ניתוח של מקטעים האלה הדגים כי ישנה שונות בין אופרוני TAD של BALO שונים וכי שונות זאת קשורה לנישה האקולוגית ממנה בודד החיידק הטורף. בעבודה זו עוד מצאתי אורתולוגים של גן הבקרה bd0108 , וכן זוהה מוטיב חלבוני המאפיין אורטולוגים של bd0108 מחיידקים טורפים לא ימיים. יתר על כן, הדגמנו שאופרון ה-TAD של .B bacteriovorus, ולכן flp1 וflp2- , נמצא תחת רגולציה של פקטור המבקר את פעילות השוטון, FliA, בעוד שflp4- אינו תחת ההשפעה של פקטור זה. בניגוד לבקטריות אחרות fliA הפך לגן מרכזי ב- .B bacteriovorus. 4 4. Introduction Predation in the microbial realm Predation between microbes is ubiquitous. As with larger organisms, predation grants access to a nutritionally-rich resource in oligotrophic environments. However, this requires overcoming the prey to be consumed. One mechanism by which bacteria prey on other bacteria is by massively secreting noxious enzymes and chemicals which have the ability to degrade surrounding prey bacteria [3-5]. The lysed prey compounds are then absorbed by the predator [4, 5]. The model for such predatory strategy is Myxococcus, a Gram-negative bacterium which secretes bacteriolytic enzymes encapsulated in membrane vesicles, which then penetrate and degrade any surrounding bacteria [3, 6]. Another example is Pseudomonas aeruginosa, that under conditions of iron starvation secretes both bacteriolytic chemicals (which degrade Staphylococcus aureus), and high affinity iron chelators (which bind iron molecules from prey degraded material)[4, 7]. This predatory strategy seems not to necessitate specific mechanisms for identifying the prey, as predation does not require close cell-cell contacts. This, in turn, guarantees access to plenty of nutrients but may also results in the loss
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