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. Ama o KR, Yeoman CJ, Ken A, Righini N, Ca bone o F, Es ada
A, e al. Habi a deg ada ion impac s black howle monkey
(Aloua a pig a) gas oin es inal mic obiomes. ISME J.
2013;7:1344–53.
5. Claus SP, Guillou H, Elle o-Sima os S, Qin J, Spo A, Ko en O,
e al. The gu mic obio a: a majo playe in he oxici y o
en i onmen al pollu an s? NPJ Biofilms Mic obiomes.
2016;2:16003.
6. Zhang A, S een TY. Gu mic obiomics—a solu ion o unloose he
go dian kno o biological e ec s o ionizing adia ion. J He ed.
2017;279:1718–22.
7. Lou enço J, Mendo S, Pe ei a R. Radioac i ely con amina ed
a eas: bioindica o species and bioma ke s o e ec in an ea ly
wa ning scheme o a p elimina y isk assessmen . J Haza d
Ma e . 2016;317:503–42.
8. Mølle AP, Mousseau TA. Biological consequences o Che nobyl:
20 yea s on. T ends Ecol E ol. 2006;21:200–7.
9. Je n o s T, Kesäniemi J, La inienko A, Mappes T, Miline sky G,
Mølle AP, e al. T ansc ip ional up egula ion o DNA damage
esponse genes in bank oles (Myodes gla eolus) inhabi ing he
Che nobyl Exclusion Zone. F on En i on Sci. 2018;5:95.
10.3389/ en s.2017.0009.
En i onmen al adia ion al e s he gu mic obiome o he bank ole Myodes gla eolus 2805
10. Eino D, Bonisoli-Alqua i A, Cos an ini D, Mousseau TA, Mølle
AP. Ionizing adia ion, an ioxidan esponse and oxida i e
damage: a me a-analysis. Sci To al En i on. 2016;548:463–71.
11. Mølle AP, Mousseau TA. S ong e ec s o ionizing adia ion
om Che nobyl on mu a ion a es. Sci Rep. 2015;5:8363.
12. Ragon M, Res oux G, Mo ei a D, Mølle AP, López-Ga cía P.
Sunligh -exposed biofilm mic obial communi ies a e na u ally
esis an o Che nobyl ionizing- adia ion le els. PLoS ONE.
2011;6:e21764.
13. Ruiz-González MX, Czi ják GÁ, Gene aux P, Mølle AP,
Mousseau TA, Heeb P, e al. Resis ance o ea he -associa ed
bac e ia o in e media e le els o ionizing adia ion nea Che no-
byl. Sci Rep. 2016;6:22969.
14. Romano skaya VA, Sokolo IG, Roki ko PV, Che naya NA.
E ec o adioac i e con amina ion on soil bac e ia in he 10-km
zone a ound he Che nobyl Nuclea Powe Plan . Mic obiology.
1998;67:226–31.
15. Mo on JT, Sande s J, Quinn RA, McDonald D, Gonzalez A,
Vázquez-Baeza Y, e al. (2017). Balance ees e eal mic obial
niche di e en ia ion. mSys ems. 2017;2. h ps://doi.o g/10.1128/
mSys ems.00162-16.
16. Langille M, Zane eld J, Capo aso JG, McDonald D, Knigh s D,
Reyes J, e al. P edic i e unc ional p ofiling o mic obial com-
muni ies using 16S RNA ma ke gene sequences. Na Bio-
echnol. 2013;31:814–21.
17. Pa ks BW, Nam E, O g E, Kos em E, No heim F, Hui ST, e al.
Gene ic con ol o obesi y and gu mic obio a composi ion in
esponse o high- a , high-suc ose die in mice. Cell Me ab.
2013;17:141–52.
18. Mølle AP, Mousseau TA. A e o ganisms adap ing o ionizing
adia ion a Che nobyl? T ends Ecol E ol. 2016;31:281–9.
19. Chesse RK, Bonda ko M, Bake RJ, Wickli e JK, Rodge s BE.
Recons uc ion o adioac i e plume cha ac e is ics along Che -
nobyl’s Wes e n T ace. J En i on Radioac . 2004;71:147–57.
20. Kozakiewicz M, Chołuj A, Kozakiewicz A. Long-dis ance
mo emen s o indi iduals in a ee-li ing bank ole popula ion:
an impo an elemen o male b eeding s a egy. Ac a The iol
(Wa sz). 2007;52:339–48.
21. Mau ice CF, Haise HJ, Tu nbaugh PJ. Xenobio ics shape he
physiology and gene exp ession o he ac i e human gu mic o-
biome. Cell. 2013;152:39–50.
22. P akash D, Gabani P, Chandel AK, Ronen Z, Singh OV. Bio -
emedia ion: a genuine echnology o emedia e adionuclides om
he en i onmen . Mic ob Bio echnol. 2013;6:349–60.
23. Chesse RK, Sugg DW, Lomakin MD, an den Bussche RA,
DeWoody JA, Jagoe CH, e al. Concen a ions and dose
a e es ima es o 134, 137 cesium and 90 s on ium in small
mammals a Cho nobyl, Uk aine. En i on Toxicol Chem.
2000;19:305–12.
24. Daniel H, Gholami AM, Be y D, Desma chelie C, Hahne H, Loh
G, e al. High- a die al e s gu mic obio a physiology in mice.
ISME J. 2014;8:295–308.
25. Macdonald DW. The encyclopedia o mammals. 3 d ed. Ox o d
Uni e si y P ess: Ox o d, UK, 2007.
26. Ko opa kin NM, Came on EA, Ma ens EC. How glycan me a-
bolism shapes he human gu mic obio a. Na Re Mic obiol.
2012;10:323–35.
27. Mølle AP, Mousseau TA. Reduced abundance o insec s
and spide s linked o adia ion a Che nobyl 20 yea s a e he
acciden . Biol Le . 2009;5. h ps://doi.o g/10.1098/ sbl.2008.
0778.
28. Da id LA, Mau ice CF, Ca mody RN, Goo enbe g DB, Bu on
JE, Wol e BE, e al. Die apidly and ep oducibly al e s he
human gu mic obiome. Na u e. 2014;505:559–63.
29. Rooks MG, Ga e WS. Gu mic obio a, me aboli es and hos
immuni y. Na Re Immunol. 2016;16:341–52.
30. Hame HM, Jonke s D, Venema K, Vanhou in S, T oos FJ,
B umme R-J. Re iew a icle: he ole o bu y a e on colonic
unc ion. Alimen Pha macol The . 2007;27:104–19.
31. Bui TPN, Ri a i J, Boe en S, de Waa d P, Plugge CM, de Vos
WM. P oduc ion o bu y a e om lysine and he Amado i p oduc
uc oselysine by a human gu commensal. Na Commun.
2015;6:10062.
32. Albe di A, Aizpu ua O, Bohmann K, Zepeda-Mendoza ML,
Gilbe MTP. Do e eb a e gu me agenomes con e apid eco-
logical adap a ion? T ends Ecol E ol. 2016;31:689–99.
2806 A. La inienko e al.