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Tom 49 Numer 2 Rok 2010 POST. MIKROBIOL., RÓ¯NORODNE FUNKCJE 2010, 40, 2, 105114 http://www.pm.microbiology.pl WYBRANYCH PIGMENTÓW BAKTERYJNYCH Krystyna I. Wolska*1, Anna M. Grudniak1, Anna Kraczkiewicz-Dowjat1, Anna Kurek1 1Zak³ad Genetyki Bakterii, Instytut Mikrobiologii, Wydzia³ Biologii, Uniwersytet Warszawski ul. Miecznikowa 1, 02-096 Warszawa Wp³ynê³o w lutym 2010 r. 1. Wstêp. 2. Pigmenty jako czynniki wirulencji. 2.1. Pseudomonas aeruginosa i piocyjanina. 2.2. Staphylococcus aureus i stafylo- ksantyna. 2.3 Inne bakterie chorobotwórcze i ich pigmenty. 3. Funkcje pigmentów nie zwi¹zane z chorobotwórczoci¹. 3.1. Fotosyn- teza. 3.2. Pozyskiwanie ¿elaza. 3.3. Ochrona przed szkodliwym dzia³aniem czynników rodowiskowych i zwi¹zków antybakteryjnych. 4. Mo¿liwoæ zastosowania pigmentów bakteryjnych w medycynie i przemyle. 5. Podsumowanie Various functions of selected bacterial pigments Abstract: Bacterial pigments are produced by numerous bacterial species. Their production gives the bacteria an advantage in their competition for environmental niches. Several pigments produced by pathogens, e.g. staphyloxanthin of S. aureus or pyocyanin of P. aeruginosa have been proved to be important factors of virulence and their modes of action are well established. In natural environment, such as soil or water, bacterial pigments are indispensable for photosynthesis. They are also able to protect bacteria against harmful effect of temperature, osmolarity, radiation and antibacterial compounds and also to help bacteria in iron acquisition via the pathways alternative to siderophores. Recently, studies have been conduced on antibacterial therapy based on pigment inhibition and the potential use of pigments in the industry and medicine, mainly as an anticancer agents. Introduction. 2. Pigments as the virulence factors. 2.1. Pseudomonas aeruginosa and pyocyanin. 2.2. Staphylococcus aureus and staphyloxanthin. 2.3. Other pathogenic bacteria and their pigments. 3. Functions of pigments other than virulence determinants. 3.1. Photosynthesis. 3.2. Acquisition of iron. 3.3. Protection against harmful environmental factors and antibacterials. 4. Possibility of medical and commercial application of bacterial pigments. 5. Summary S³owa kluczowe: pigmenty bakteryjne, czynniki wirulencji, fotosynteza, pozyskiwanie ¿elaza, ochrona przed stresem Key words: bacterial pigments, virulence factors, photosynthesis, iron acquisition, stress protection 1. Wstêp menty bakteryjne maj¹ aktywnoæ antybiotyczn¹ oraz, co bardzo wa¿ne, s¹ czynnikami wirulencji chorobo- Wiele gatunków bakterii nale¿¹cych do kilku ty- twórczych bakterii. Te wszystkie naturalne funkcje pów taksonomicznych posiada zdolnoæ do syntezy bakteryjnych barwników bêd¹ omówione w nastêp- zwi¹zków barwnych. Gatunki barwne, nie tylko bak- nych rozdzia³ach tego opracowania. Nale¿y tak¿e teryjne, maj¹ istotn¹ przewagê w naturalnym ro- zaznaczyæ, ¿e kolorystyka poszczególnych gatunków dowisku bytowania, co jest szczególnie widoczne znajduje odbicie w ich nazwie, na przyk³ad Staphy- w przypadku zwierz¹t krêgowych, których jaskrawe lococcus aureus (gronkowiec z³ocisty) lub Chromo- ubarwienie zwiêksza atrakcyjnoæ osobników dla p³ci bacterium violaceum (gatunek bakteryjny o zabarwie- przeciwnej, u³atwia kamufla¿ a tak¿e odstrasza poten- niu fioletowym). Pigmentacja jest tak¿e cech¹ u³atwia- cjalnych wrogów. Wszystkie te korzyci zwi¹zane s¹ j¹c¹ identyfikacjê danego gatunku, szczególnie istotn¹ ze zdolnoci¹ zwierz¹t do percepcji ró¿nych kolorów, w diagnostyce klinicznej. co a priori jest niemo¿liwe u bakterii. Mimo tego, Badania funkcji barwników oraz szlaków ich bio- korzyci, które czerpi¹ barwne bakterie s¹ liczne i ró¿- syntezy w komórce bakteryjnej prowadzone s¹ inten- norodne, a ich przewaga selekcyjna nad gatunkami sywnie od oko³o 20 lat. Eksperymenty wykonuje siê lub mutantami bezbarwnymi jest znaczna. Korzyci te zarówno in vivo, g³ównie przez porównanie fenotypu polegaj¹ na: zdobywaniu pokarmu i energii (bakterie bezbarwnego mutanta z barwnym szczepem wyjcio- fotosyntetyzuj¹ce), pozyskiwaniu ¿elaza ze rodowi- wym, jak i in vitro, badaj¹c wp³yw izolowanych pig- ska, ochronie przed szkodliwym dzia³aniem wiat³a mentów na rodowisko (w wypadku bakterii chorobo- widzialnego o du¿ym natê¿eniu, promieniowania ultra- twórczych na komórki zainfekowanego gospodarza). fioletowego, ekstremalnych temperatur, jak równie¿ W ostatnich latach sta³o siê mo¿liwe wykorzystanie zwi¹zków o dzia³aniu antybakteryjnym, produkowa- w tych badaniach technik stosowanych w biologii nych przez inne organizmy. Poza tym niektóre pig- molekularnej i biotechnologii, co przybli¿a dog³êbne * Autor korespondencyjny: Zak³ad Genetyki Bakterii, Instytut Mikrobiologii, Wydzia³ Biologii, Uniwersytet Warszawski, ul. Miecznikowa 1, 02-096 Warszawa, tel.: (22) 554 13 02, e-mail: [email protected] 106 KRYSTYNA I. WOLSKA, ANNA M. GRUDNIAK, ANNA KRACZKIEWICZ-DOWJAT, ANNA KUREK poznanie zarówno regulacji syntezy pigmentów jak a szczególnie P. aeruginosa, stanowi¹ du¿e zagro¿e- i mechanizmów ró¿norodnego (plejotropowego) ich nie zdrowotne. dzia³ania na komórki organizmów wy¿szych oraz mo- P. aeruginosa wytwarza cztery pigmenty, z których lekularnych podstaw udzia³u barwników w chorobo- najwa¿niejszym jest piocyjanina, koloru niebiesko- twórczoci bakterii. zielonego. Barwnik ten jest wydzielany poza komór- kê, nadaj¹c charakterystyczne szmaragdowe zabar- wienie pod³o¿u hodowlanemu lub wydzielinie p³ucnej 2. Pigmenty jako czynniki wirulencji osób zaka¿onych tym patogenem. Innymi barwnikami P. aeruginosa s¹: zielona, zdolna do fluorescencji 2.1. Pseudomonas aeruginosa i piocyjanina fluoresceina (piowerdyna), czerwona piorubina oraz br¹zowa melanina. Barwa dwóch ostatnich bywa Gramujemne pa³eczki, P. aeruginosa (klasa Gam- maskowana przez zielony kolor piocyjaniny. Piocyja- maproteobacteria, rodzina Psedomonadaceae) cha- nina (1-hydroksy-5-metylofenozyna) jest zwiterjonem rakteryzuj¹ siê zdolnoci¹ do przeprowadzania bardzo (Rys. 1A). T¹ nazw¹ okrelane s¹ zwi¹zki, w których licznych reakcji biochemicznych, które nale¿¹ do w jednej cz¹steczce i blisko siebie znajduj¹ siê grupy ró¿norodnych szlaków metabolicznych. W zwi¹zku na³adowane dodatnio i ujemnie. Taka struktura umo¿- z tym, bakterie te mo¿e rosn¹æ w ró¿nych rodowis- liwia swobodne przechodzenie cz¹stek przez b³ony kach i maj¹ zdolnoæ do infekcji wielu gatunków biologiczne. Piocyjnina jest wa¿nym czynnikiem wi- organizmów eukariotycznych, od ameby do cz³owieka. rulencji P. aeruginosa. Powoduje znaczny wzrost stê- U ludzi wywo³uj¹ liczne schorzenia, w tym: zapalenie ¿enia reaktywnych form tlenu RFT (ang. reactive ucha rodkowego, zapalenie stawów, zapalenie wsier- oxygen substances ROS) w komórkach eukariotycz- dzia, choroby uk³adu moczowego, zaka¿enia ran, na nych. Ma to zwi¹zek ze zdolnoci¹ tego barwnika do przyk³ad powsta³ych w wyniku poparzeñ. Ogromny przenoszenia elektronów ze zwi¹zków zredukowa- potencja³ chorobotwórczy P. aeruginosa zwi¹zany jest nych, np. glutationu, na tlen, a to prowadzi do obni¿e- z syntez¹ przez tê bakteriê kilku czynników wirulen- nia w eukariotycznej komórce stê¿enia antyoksydan- cji, z których najwa¿niejszymi s¹ proteazy, hemolizy- tów z jednoczesnym zwiêkszeniem stê¿enia zwi¹zków ny, adhezyny i egzotoksyny. Te ostatnie odpowiadaj¹ silnie utleniaj¹cych, którymi s¹ RFT [42]. Obser- za martwicê tkanek i problemy z leczeniem zainfeko- wowano równie¿ zahamowanie aktywnoci katalazy wanych ran. Egzotoksyny s¹ transportowane bezpo- przez ten barwnik [41]. Wszystkie RFT zawieraj¹ rednio do komórek eukariotycznych przez system w cz¹steczkach reaktywne, niesparowane elektrony. sekrecji typu III, który, jako taki, mo¿e byæ tak¿e uwa- Przyk³adami tych zwi¹zków s¹ wolne rodniki, nad- ¿any za czynnik wirulencji tej bakterii [61]. Jednak, tlenki oraz tlen singletowy (O = O). Ograniczona iloæ mimo obecnoci tak licznych czynników odpowiedzial- RFT powstaje w komórkach eukariotycznych jako nych za patogennoæ, gatunek ten rzadko infekuje osob- naturalne produkty metabolizmu i pe³ni wa¿ne funk- niki zdrowe, a to ze wzglêdu na s³ab¹ zdolnoæ do ko- cje w oksydatywnej, mitochondrialnej fosforylacji, lonizacji i niszczenia komórek nab³onka. Dlatego te¿ apoptozie czy krzepniêciu krwi [35]. Zwiêkszenie stê- P. aeruginosa jest klasycznym przyk³adem patogenu ¿enia RFT bêd¹ce typowym skutkiem wielu infekcji oportunistycznego, gronego dla osób z obni¿on¹ od- bakteryjnych, nazywane stresem oksydacyjnym, jest pornoci¹, z czym wi¹¿¹ siê ró¿norodne zaka¿enia wa¿nym czynnikiem obrony gospodarza przed infe- szpitalne, których jest przyczyn¹. Do czynników ryzy- kuj¹cymi patogenami (patrz ni¿ej). Jednak masywny, ka zaka¿eniem P. aeruginosa nale¿¹: AIDS, choroba zwi¹zany z aktywnoci¹ piocyjaniny stres oksyda- nowotworowa, cukrzyca, a zw³aszcza mukowiscydoza. cyjny po infekcji P. aeruginosa ma wielorakie skutki Wolno ¿yj¹ce komórki P. aeruginosa s¹ niezwykle destrukcyjne. Olbrzymie zwiêkszenie RFT w komór- ruchliwe dziêki obecnoci d³ugiej, pojedynczej rzêski kach ¿ernych neutrofilach prowadzi do ich apop- umiejscowionej na biegunie bakterii. Gatunek ten tozy, zanotowano równie¿ zmniejszenie wydzielania ma tak¿e zdolnoæ do wzrostu w postaci biofilmu. cytokin, co skutkuje supresj¹ uk³adu immunologicz- Pojedyncze komórki tworz¹ce tê strukturê s¹ zle- nego [2]. Oksydacyjny stres zaburza tak¿e homeosta- pione, i przez to unieruchomione, przez wielocukier, zê jonów wapnia, a co za tym idzie sekrecjê luzu, alginian, tworz¹cy tzw. macierz biofilmu [44]. Bio- rytmiczny ruch rzêsek w górnych drogach oddecho- filmy tworz¹ siê na granicy
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