Environmental radiation alters the gut microbiome of the bank vole Myodes glareolus

This is a sel -a chi ed e sion o an o iginal a icle. This e sion may di e om he o iginal in pagina ion and ypog aphic de ails. Au ho (s): Ti le: Yea : Ve sion: Copy igh : Righ s: Righ s u l: Please ci e he o iginal e sion: CC BY 4.0 h ps://c ea i ecommons.o g/licenses/by/4.0/ En i onmen al adia ion al e s he gu mic obiome o he bank ole Myodes gla eolus © 2018 he Au ho s Published e sion La inienko, An on; Mappes, Tapio; Tukalenko, Eugene; Mousseau, Timo hy A.; Mølle , Ande s P.; Knigh , Rob; Mo on, James T.; Thompson, Luke R.; Wa s, Phillip C. La inienko, A., Mappes, T., Tukalenko, E., Mousseau, T. A., Mølle , A. P., Knigh , R., Mo on, J. T., Thompson, L. R., & Wa s, P. C. (2018). En i onmen al adia ion al e s he gu mic obiome o he bank ole Myodes gla eolus. ISME Jou nal, 12(11), 2801-2806. h ps://doi.o g/10.1038/s41396-018-0214-x 2018 The ISME Jou nal (2018) 12:2801–2806 h ps://doi.o g/10.1038/s41396-018-0214-x BRIEF COMMUNICATION En i onmen al adia ion al e s he gu mic obiome o he bank ole Myodes gla eolus An on La inienko 1●Tapio Mappes2●Eugene Tukalenko2,3 ●Timo hy A. Mousseau4●Ande s P. Mølle 5● Rob Knigh 6,7,8 ●James T. Mo on6,7 ●Luke R. Thompson 9,10 ●Phillip C. Wa s1 Recei ed: 16 Janua y 2018 / Re ised: 16 May 2018 / Accep ed: 11 June 2018 / Published online: 9 July 2018 © The Au ho (s) 2018. This a icle is published wi h open access Abs ac Gu mic obio a composi ion depends on many ac o s, al hough he impac o en i onmen al pollu ion is la gely unknown. We used amplicon sequencing o bac e ial 16S RNA genes o quan i y whe he an h opogenic adionuclides a Che nobyl (Uk aine) impac he gu mic obiome o he bank ole Myodes gla eolus. Exposu e o ele a ed le els o en i onmen al adionuclides had no de ec able e ec on he gu communi y ichness bu was associa ed wi h an almos wo- old inc ease in he Fi micu es:Bac e oide es a io. Animals inhabi ing uncon amina ed a eas had ema kably simila gu communi ies i espec i e o hei p oximi y o he nuclea powe plan . Hence, samples could be classified o high- adia ion o low- adia ion si es based solely on mic obial communi y wi h >90% accu acy. Radia ion-associa ed bac e ia had dis inc in e ed unc ional p ofiles, including pa hways in ol ed in deg ada ion, assimila ion and anspo o ca bohyd a es, xenobio ics biodeg ada ion, and DNA epai . Ou esul s sugges ha exposu e o en i onmen al adionuclides significan ly al e s e eb a e gu mic obio a. In oduc ion Ou unde s anding o he ac o s ha shape gu mic obiome is domina ed by s udies o humans [1] o labo a o y animals [2]. In con as , he p ocesses ha de e mine he composi- ion o gu mic obiomes in wildli e a e poo ly known bu include, o example, hos die (in wild mice, [3]) and habi a quali y (in p ima es, [4]). Whe he pe sis en pollu an s impac he gu mic obiomes o wildli e in hei na u al habi a is no known, al hough exposu e o a ious chemicals, hea y me als [5], o ionizing adia ion [6] can change he gu mic obio a composi ion o labo a o y oden s. Pollu ion by adionuclides is a po en ial sou ce o gen- o oxici y o humans and wildli e [7]. Animals inhabi ing he Che nobyl Exclusion Zone (CEZ) p o ide he bes -s udied model o he biological impac o exposu e o *An on La inienko An on.La inienko@oulu.fi 1Depa men o Ecology and Gene ics, Uni e si y o Oulu, 90014 Oulu, Finland 2Depa men o Biological and En i onmen al Science, Uni e si y o Jy äskylä, 40014 Jy äskylä, Finland 3Ins i u e o Biology and Medicine, Ta as She chenko Na ional Uni e si y o Kyi , Kyi 03022, Uk aine 4Depa men o Biological Sciences, Uni e si y o Sou h Ca olina, Columbia, SC 29208, USA 5Ecologie Sys e ma ique E olu ion, Uni e si é Pa is-Sud, CNRS, Ag oPa isTech, Uni e si é Pa is-Saclay, 91405 O say Cedex, F ance 6Depa men o Pedia ics, Uni e si y o Cali o nia San Diego, La Jolla, CA 92037, USA 7Depa men o Compu e Science and Enginee ing, Uni e si y o Cali o nia San Diego, La Jolla, CA 92037, USA 8Cen e o Mic obiome Inno a ion, Uni e si y o Cali o nia San Diego, La Jolla, CA 92037, USA 9Depa men o Biological Sciences and No he n Gul Ins i u e, Uni e si y o Sou he n Mississippi, Ha iesbu g, MS, USA 10 A lan ic Oceanog aphic and Me eo ological Labo a o y, Na ional Oceanic and A mosphe ic Adminis a ion, s a ioned a Sou hwes Fishe ies Science Cen e , Na ional Ma ine Fishe ies Se ice, La Jolla, CA, USA Elec onic supplemen a y ma e ial The online e sion o his a icle (h ps://doi.o g/10.1038/s41396-018-0214-x) con ains supplemen a y ma e ial, which is a ailable o au ho ized use s. 1234567890();,: 1234567890();,: en i onmen al adionuclides [8]. De imen al e ec s o a ch onic exposu e o adia ion on wildli e include ele a ed DNA damage [7] and up egula ion o DNA epai genes [9], inc eased oxida i e s ess [10], and an inc ease in mu a ion a e [11]. Any ye , li le is known abou he e ec s o en i onmen al adia ion on mic oo ganisms. While some bac e ia om he CEZ ha e a capaci y o adap a ion o en i onmen al adioac i i y [12,13], o he s udies epo ed a decline in di e si y wi h inc eased adia ion exposu e [14]. Howe e , no s udy has quan ified he impac o exposu e o en i onmen al adia ion on hos -associa ed gu mic obial communi ies in wild animals. Me hods and esul s To quan i y whe he exposu e o en i onmen al adia ion impac s he gu mic obial communi y o a wild oden , he bank ole Myodes gla eolus, we sequenced he V4 egion o he 16S RNA genes om he gu mic obio a o 137 bank oles (Supplemen a y Table 1). Bank oles we e sampled om h ee s udy a eas ha di e ed in he le els o en i - onmen al adia ion, and ep esen ed wo ea men s: (1) high (CH n=63, mean =30.1 µS /h) and (2) low (CL n=43, mean =0.25 µS /h and KL n=31, mean =0.33 µS /h) adia ion con amina ion (Supplemen a y Figu e 1, see de ailed desc ip ions o he me hods and esul s in he Sup- plemen a y In o ma ion). Nei he communi y ichness no e enness di e ed significan ly (P> 0.05) be ween samples g ouped by s udy a ea (all pai wise compa isons o CH, CL, and KL) o we e a ec ed by hos sex (Supplemen a y Figu e 2, Supplemen a y Table 2). Significan (P=0.001) di e ences in be a di e si y (Fig. 1d, Supplemen a y Fig- u e 3) we e obse ed be ween CH and bo h CL and KL, bu no due o e ec s o sex, a con amina ion by sex in e ac ion, o due o a ia ion in bank ole body mass, head wid h (a p oxy o age), o g a idi y s a us ( o emales) (Supple- men a y Table 3). Radia ion, bu no indi idual le el p edic o s such as sex, body mass, o head wid h (a p oxy o age), was iden ified as a significan p edic o o he abundance o Bac e oide es (P=0.0001), Fi micu es (P< 0.0001), and P o eobac e ia (P=0.001) (Supplemen a y Table 4). No ably, we ound an almos wo- old, significan (P< 0.001) dec ease in he a io o Fi micu es o Bac e oide es (F:B) sequences om 1.7 in he adioac i ely con amina ed CH a ea o <0.9 in he uncon amina ed a eas CL (F:B =0.87) and KL (F:B = 0.78) (Fig. 1a, b, Supplemen a y Tables 5 and 6). This pa e n was appa en ac oss eplica e si es (Supplemen a y Figu e 4) and axonomic le els (Fig. 1c, Supplemen a y Table 6) in each ea men , indica ing ha he F:B a io in bank ole gu s is associa ed wi h he le el o en i onmen al adia ion. These ends we e also e ified beyond he phylum le el in independen p edic ions by using a combina ion o pa ial leas squa es (PLS) eg ession and balances [15] (Supplemen a y In o ma ion). The a ea-based balance could di e en ia e be ween he CH and he CL/KL a eas (AUC = 0.957, F-s a is ic =204.7, P=9.18 × 10−29), wi h a mean c oss- alida ion p edic ion accu acy o 0.917 (Fig. 2a, b, Supplemen a y Tables 7 and 8). This pa e n was obus , e en when he analysis was limi ed o 10 samples pe s udy a ea (Supplemen a y Table 8). Using he adia ion-based balance, we could p edic adia ion le els (Pea son’s =–0.766, P=1.46 × 10−27) (Supplemen a y Figu e 5, Supplemen a y Tables 9 and 10, see Supplemen a y In o - ma ion o esul s). We used PICRUS [16] o make unc ional p edic ions o bank ole gu mic obio a. Analyses using bo h PLS and K uskal–Wallis iden ified co e bac e ial unc ions s ongly associa ed wi h he s udy a ea (CH s. CL/KL) (Fig. 2c, Supplemen a y Table 11). The s iking simila i y in he unc ional p ofiles o he uncon amina ed a eas, despi e hei spa ial sepa a ion (Supplemen a y Figu e 1) and po en ial habi a di e ences, and he con as be ween he uncon a- mina ed and con amina ed a eas ein o ces he ele ance o adioac i i y on gu mic obial communi y unc ion. Discussion Exposu e o an h opogenic adionuclide con amina ion p esen s di e se isks o li ing o ganisms [7], bu i s e ec s on gu mic obio a a e unknown. Ou analysis o he gu mic obio a o a wild e eb a e exposed o en i onmen al adia ion unco e majo changes o he gu mic obiome composi ion and in e ed unc ional p ofiles. Ex ensi e in e -indi idual a ia ion in gu mic obio a p ofiles (Fig. 1d) is a ypical ea u e o hos he e ogenei y in ac o s such as age, geno ype [17], sex, and die [3]. While he use o di e se sampling loca ions will likely add noise, i is an essen ial pa o ou expe imen al design ha he ea men ( adia ion) e ec is obse ed ou side one specific loca ion such as he Red Fo es (one o he mos con- amina ed si es in he CEZ) [18]. No o he po en ial p e- dic o s (e.g. body mass, age, sex) o gu bac e ial abundance we e ound, in con as o he gene al e ec o adia ion exposu e (Supplemen a y Tables 3 and 4). The CEZ p esen s a mosaic o adionuclides deposi ion, whe e con amina ed and uncon amina ed a eas can be sepa a ed by ~1.5 km [19]. Bank oles may mo e up o 1 km wi hin a b eeding season [20], and hus indi iduals om uncon amina ed a eas wi hin he CEZ (CL), bu no indi iduals in he a ea a ound Kyi (KL), ha e he oppo - uni y o be exposed o adionuclides p io o cap u e [9]; wi h his in mind, he di e ences in gu mic obio a 2802 A. La inienko e al. composi ion be ween CH and CL, and he simila i y be ween CL and KL, a e s iking. The implica ion is ha he gu mic obial communi y esponds apidly and a a small scale o hos habi a , consis en wi h labo a o y expe imen s ha show how ex e nal s imuli can d i e changes in gu mic obiome wi hin a ew days [5,21]. Changes in he gu communi y composi ion migh eflec bac e ial adiosensi i i y. In e es ingly, some mem- be s o he Desul o ib ionaceae can ole a e high adia ion le els (CH) and ha e a po en ial o bio emedia ion o adionuclides [22], aising he possibili y ha i has a de oxi ying ole in he bank ole gu . I is no known whe he he compa a i ely low and ch onic dose o adio- nuclides (~2–10 mGy/d) ha wildli e expe ience wi hin he CEZ [23] could impose di e en ial mo ali y wi hin he gu bac e ial communi y. Howe e , en ichmen o DNA epai pa hways (Fig. 2c, Supplemen a y Table 11) in con amina ed a eas implies an inc eased e o o epai bac e ial DNA associa ed wi h ele a ed le els o en i on- men al adia ion. Selec ion o a mo e dis inc gu mic obio a in adio- ac i ely con amina ed a eas p ima ily eflec s a eplacemen o Bac e oide es by Fi micu es. In a b oad con ex , he F:B a io wi hin he gu is a ec ed by die [2,17] and is asso- cia ed wi h bac e ial me abolic po en ial [24]. Bank oles ha e a ca holic die ha includes seeds, lea es, oo s, g asses, ui and ungi and, occasionally, insec s, and o he in e eb a es [25]. Gu communi ies domina ed by Bac e - oide es can exploi a ious die a y subs a es [26] and hus, could allow e ficien use o di e se oods, indica ing he Fig. 1 Radia ion-associa ed di e ences in bank ole gu mic obio a communi y composi ion and be a di e si y. aRela i e abundances o h ee majo bac e ial phyla and bFi micu es o Bac e oide es a io (F:B) in he gu mic obio a o bank oles inhabi ing a eas ha di e in le els o en i onmen al adia ion. As e isks indica e significan di - e ences among a eas con amina ed (CH) and uncon amina ed (CL) wi h adionuclides wi hin he Che nobyl Exclusion Zone and an uncon amina ed a ea nea Kyi (KL), Uk aine (Bon e oni-co ec ed K uskal–Wallis es ). ***P< 0.001. cMean ela i e abundance o bac e ial axa a o de le el in he bank ole gu mic obio a. Unas- signed axa (<2.3%) a e no shown. dPCoA on B ay–Cu is dissim- ila i y dis ances be ween bank ole gu mic obio a p ofiles among he h ee s udy a eas. Each poin ep esen s a single sample, shape indi- ca es hos sex, colo ed acco ding o s udy a ea: CH, ed (n=63); CL, blue (n=43); KL, g een (n=31). Ellipses ep esen a 95% CI a ound he clus e cen oid. Clus e ing significance by ea men g oup was de e mined by adonis, P< 0.001 En i onmen al adia ion al e s he gu mic obiome o he bank ole Myodes gla eolus 2803 Fig. 2 Balance T ees analysis and PICRUS unc ional p edic ions o he bank ole gu mic obio a. Pa ial leas squa es (PLS) balance analysis o aa ea-di e en ia ed OTUs (shown a e he p opo ions in he wo g oups o he op 10 OTUs in each g oup based on PLS sco e) and bclassifica ion o samples o s udy a eas based on OTU compo- si ion. cHea map o he KEGG le el-3 unc ional pa hways ha significan ly di e ed be ween con amina ed (CH) and bo h uncon a- mina ed a eas (CL and KL). Pa hway coun s we e no malized as implemen ed in supe hea 0.1.0 R package, abundance o each pa hway is indica ed by a g adien o colo om ed (low abundance) o blue (high abundance). Full lis s o pa hways associa ed wi h adia ion exposu e can be ound in Supplemen a y Table 11 2804 A. La inienko e al. likely adap i e s a e in na u e. Fi micu es end o me abolize o he wise indiges ible esis an s a ch (Clos idiales, Lac- obacillales) and plan cell wall glycans (Ruminococcaceae, Lachnospi aceae)[26]. Bank oles inhabi ing adioac i ely con amina ed a eas (CH) hus exhibi an appa en die a y shi , which is also suppo ed by he in e ed me abolic unc ions (Fig. 2c, Supplemen a y Table 11). The e a e no de ailed biodi e si y su eys o he CEZ and su ounding a eas, bu a change in die associa ed wi h en i onmen al adioac i i y migh eflec he educed abundance o a h opods in he mo e con amina ed a eas wi hin he CEZ [27]. Al e na i ely, bank oles inhabi ing CH a eas migh ac i ely inc ease he amoun o plan -based oods o p o- duce mo e o he end p oduc s o e men a ion o die a y fibe (sho -chain a y acids, SCFAs) [28]. SCFAs can con e addi ional benefi s o he hos beyond ene gy ha es by ac ing as physiological and immune egula o s [26,29]. Gu bac e ia ha p oduce bu y a e may p o ec agains geno oxins as his SCFA a ec s DNA epai sys ems and an ioxidan le els [30] and can educe oxida- i e s ess ha is widely associa ed wi h animals inhabi ing con amina ed a eas wi hin he CEZ [10]. Bu y a e is p o- duced by many Fi micu es, specifically membe s o he Clos idiales, Ruminococcaceae and Lachnospi aceae [31], ha a e significan ly mo e abundan in CH, bu is a ely associa ed wi h he SCFA p ofiles o Bac e oide es [26]. En ichmen o Fi micu es (Fig. 1a, b, Supplemen a y Table 6) hus is a plausible me hod o mi iga ing e ec s o ele a ed oxida i e s ess concomi an wi h inhabi ing an a ea con amina ed by adionuclides. This hypo hesis wa - an s u he s udies ha could quan i y SCFAs p ofiles and ho oughly assess hos die . In conclusion, bank oles exposed o an h opogenic en i onmen al adia ion expe ience subs an ial changes in he composi ion o hei gu mic obio a and majo changes in bac e ial unc ion. Gu mic obial composi ion can acil- i a e adap a ion [32], and migh be an impo an componen o moun ing an e ec i e esponse o condi ions wi hin he CEZ. The posi i e and nega i e adap i e and heal h con- sequences o changes o wildli e gu mic obio a emain o be quan ified. Acknowledgemen s We a e g a e ul o Gennadi Miline sky, Igo Chizhe sky, Se hii Ki eye , Ana oly Noso sky, and Maksym I a- nenko o logis ic suppo and help in o ganizing fieldwo k. Ka i Ki isaa i, Sofia Sanchez, Zbyszek Bo a yński, and Jenni Kesäniemi p o ided assis ance du ing ma e ial collec ion. The Finnish Cen e o Scien ific Compu ing (CSC), and pe sonally Kimmo Ma ila, p o ided in aluable compu ing esou ces and echnical suppo . The p ojec was unded by he Academy o Finland (p ojec numbe s 287153 and 268670, o PCW and TM) and by an open- esea ch doc o al p og am awa d ( o AL) om he Uni e si y o Oulu G adua e School. Addi- ional suppo o TAM was p o ided by he Samuel F eeman Cha i- able T us and by he Samuel Law ence Founda ion o LRT. JTM was suppo ed unde NSF-GRFP DGE-1144086. Au ho con ibu ions PCW, TM, and AL concei ed he p ojec design; AL, ET, TM, and PCW conduc ed field su eys and sample collec ion o he expe imen s. AL pe o med labo a o y wo k and comple ed sequence analysis, wi h addi ional bioin o ma ics suppo p o ided by PW, LRT, JTM, and RK a la e phases. AL w o e he manusc ip wi h significan con ibu ions om PCW, LRT, JTM, TAM, and APM and c i ical inpu om all o he au ho s. The unde s had no ole in his s udy design, da a collec ion and analysis, decision o publish, o p epa a ion o he manusc ip . Compliance wi h e hical s anda ds Conflic o in e es The au ho s decla e ha hey ha e no conflic o in e es . Open Access This a icle is licensed unde a C ea i e Commons A ibu ion 4.0 In e na ional License, which pe mi s use, sha ing, adap a ion, dis ibu ion and ep oduc ion in any medium o o ma , as long as you gi e app op ia e c edi o he o iginal au ho (s) and he sou ce, p o ide a link o he C ea i e Commons license, and indica e i changes we e made. The images o o he hi d pa y ma e ial in his a icle a e included in he a icle’s C ea i e Commons license, unless indica ed o he wise in a c edi line o he ma e ial. I ma e ial is no included in he a icle’s C ea i e Commons license and you in ended use is no pe mi ed by s a u o y egula ion o exceeds he pe mi ed use, you will need o ob ain pe mission di ec ly om he copy igh holde . To iew a copy o his license, isi h p://c ea i ecommons. o g/licenses/by/4.0/. Re e ences 1. Ya sunenko T, Rey FE, Mana y MJ, T ehan I, Dominguez-Bello MG, Con e as M, e al. Human gu mic obiome iewed ac oss age and geog aphy. Na u e. 2012;486:222–7. 2. Ca mody RN, Ge be GK, Lue ano JM, Ga i DM, Somes L, S enson KL, e al. Die domina es hos geno ype in shaping he mu ine gu mic obio a. Cell Hos Mic obe. 2015;17:72–84. 3. Mau ice CF, Cl Knowles S, Ladau J, Polla d KS, Fen on A, Pede sen AB, e al. Ma ked seasonal a ia ion in he wild mouse gu mic obio a. ISME J. 2015;9:2423–34. 4. 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