S anda ds in Genomic Sciences (2012) 7:59-69 DOI:10.4056/sigs.3036810
The Genomic S anda ds Conso ium
Comple e genome sequence o Te iglobus saanensis ype
s ain SP1PR4T, an Acidobac e ia om und a soil
Suman R. Rawa 1*, Minna K. Männis ö2, Valen in S a o oy o 3, Lynne Goodwin5, Ma
Nolan6 Lau en Hause 4, Mi iam Land4, Ka en Wals on Da enpo 5, Tanja Woyke6 and Max
M. Häggblom1
1 Depa men o Biochemis y and Mic obiology, Ru ge s, The S a e Uni e si y o New
Je sey, New B unswick, New Je sey, 08901-8520, USA
2 Finnish Fo es Resea ch Ins i u e, Ro aniemi, Finland
3 Depa men o Cell Biology and Neu oscience, Ru ge s, The S a e Uni e si y o New
Je sey, Pisca away, New Je sey, USA.
4 Oak Ridge Na ional Labo a o y, Oak Ridge, Tennessee, USA
5 Los Alamos Na ional Labo a o y, Bioscience Di ision, Los Alamos, New Mexico, USA
6 DOE Join Genome Ins i u e, Walnu C eek, Cali o nia, USA
*Co esponding au ho : Suman R. Rawa ( awa @aesop. u ge s.edu)
Keywo ds: cold adap ed, acidophile, und a soil, Acidobac e ia
Te iglobus saanensis SP1PR4T is a no el species o he genus Te iglobus. T. saanensis is o
ecological in e es because i is a ep esen a i e o he phylum Acidobac e ia, which a e
dominan membe s o bac e ial soil mic obio a in A c ic ecosys ems. T. saanensis is a cold-
adap ed acidophile and a e sa ile he e o oph u ilizing a sui e o simple suga s and complex
polysaccha ides. The genome con ained an abundance o genes assigned o me abolism and
anspo o ca bohyd a es including gene modules encoding o ca bohyd a e-ac i e enzyme
(CAZyme) amily in ol ed in b eakdown, u iliza ion and biosyn hesis o di e se s uc u al
and s o age polysaccha ides. T. saanensis SP1PR4T ep esen s he i s membe o genus
Te iglobus wi h a comple ed genome sequence, consis ing o a single eplicon o 5,095,226
base pai s (bp), 54 RNA genes and 4,279 p o ein-coding genes. We in e ha he physiology
and me abolic po en ial o T. saanensis is adap ed o allow o esilience o he nu ien -
de icien condi ions and luc ua ing empe a u es o A c ic und a soils.
In oduc ion
S ain SP1PR4T (= DSM 23119 = ATCC BAA-
1853) is he ype s ain o Te iglobus saanensis.
I is second o wo alidly asc ibed species o he
genus Te iglobus, wi h T. oseus i s isola ed
om ag icul u al soils in 2007 [1]. T. saanensis
SP1PR4T was isola ed om A c ic und a soil col-
lec ed om a wind exposed si e o Saana jeld,
no h-wes e n Finland (69°01’N, 20°50’E) [2,3].
The species name saanensis (sa.a.nen' sis. N.L.
masc. adj. saanensis) pe ains o Moun Saana in
Finland.
Acidobac e ia a e ound in di e se soil en i on-
men s and a e widely dis ibu ed in A c ic and
bo eal soils [4-8]. Howe e , ela i ely li le is s ill
known abou hei me abolic po en ial and
ecological oles in hese habi a s. Despi e a la ge
collec ion o Acidobac e ia 16S RNA gene se-
quences in da abases ha ep esen di e se
phylo ypes om a ious habi a s, ew ha e been
cul i a ed and desc ibed. Acidobac e ia ep esen
26 phylogene ic subdi isions based on 16S RNA
gene phylogeny [9] o which subdi isions 1, 3, 4
and 6 a e mos commonly de ec ed in soil en i-
onmen s [10]. The abundance o Acidobac e ia
has been ound o co ela e wi h soil pH [2,10,11]
and ca bon [1,12,13] wi h subdi ision 1
Acidobac e ia being mos abundan in sligh ly
acidic soils. The phylogene ic di e si y, ubiqui y
and abundance o his g oup sugges ha hey
play impo an ecological oles in soils.
Te iglobus saanensis ype s ain SP1PR4T
60 S anda ds in Genomic Sciences
Ou p e ious s udies on bac e ial communi y p o-
iling om A c ic alpine und a soils o no he n
Finland ha e shown ha Acidobac e ia domina e
in he acidic und a hea hs [2] and a e mul iple
eeze- haw cycles [6]. Using selec i e isola ion
echniques, including eezing soils a -20°C o 7
days, we ha e been able o isola e se e al slow
g owing and as idious s ains o Acidobac e ia.
On he basis o phylogene ic, pheno ypic and
chemo axonomic da a, including 16S RNA, poB
gene sequence simila i y and DNA–DNA hyb idi-
za ion, s ain SP1PR4T was classi ied as a no el
species o he genus Te iglobus [3]. He e, we
summa ize he physiological ea u es oge he
wi h he comple e genome sequence and anno a-
ion o Te iglobus saanensis SP1PR4T.
Classi ica ion and ea u es
Wi hin he genus Te iglobus, wo species a e as-
c ibed wi h alidly published names, T. saanensis
SP1PR4T [3] isola ed om A c ic und a soils and T.
oseus KBS 63T (DSM 18391) isola ed om ag icul-
u al soils (KBS-LTER si e) [1]. Sea ching he NCBI
non- edundan nucleo ide da abase o homology
o 16S RNA gene sequence o T. saanensis SP1PR4T
iden i ied 10 cul u ed and 20 uncul u ed s ains
ha we e unclassi ied, wi h ≥97% 16S RNA se-
quence iden i y. Phylogene ic ee based on 16S
RNA gene depic ing he posi ion o T. saanensis
SP1PR4T ela i e o he o he ype s ains wi hin
he amily Acidobac e iaceae is shown in Figu e 1.
T. saanensis SP1PR4T is dis inc ly clus e ed in o a
sepa a e b anch wi h T. oseus KBS 63T
(DQ660892) [1], as i s closes desc ibed ela i e
(97.1% 16S RNA sequence iden i y). S ain
SP1PR4T showed ~95% 16S RNA gene iden i y o
ou s ains in he genus G anulicella isola ed om
und a soils, namely “G. und icola” (95.9%), “G.
sapmiensis” (95.8%), “G. mallensis” (95.5%) and “G.
a c ica” (94.9%) [3,15] (Figu e 1).
S ain SP1PR4T g ows a pH 4.5-7.5 wi h an op i-
mum a 6.0 and a empe a u es o +4 o +30°C
wi h an op imum o +25°C on R2 medium [3]. On
R2 aga , s ain SP1PR4T o ms small, ci cula , con-
ex colonies wi h a diame e o app oxima ely 1
mm. The pigmen a ies om ligh beige o ligh
pink depending on he age o he cul u e. Cells o
s ains SP1PR4T a e G am-nega i e, non-spo e-
o ming, non-mo ile ae obic ods wi h a leng h o
1.5– 3.0 µm and a diame e o 0.5–0.7 µm. The cell-
wall s uc u e in ul a hin sec ions o elec on mi-
c og aphs o cells o s ain SP1PR4T demons a es
nume ous ou e -memb ane esicles (Table 1, Fig-
u e 2).
S ain SP1PR4T u ilized ca bon subs a es o
g ow h which include cellobiose, D- uc ose, D-
galac ose, D-glucose, lac ose, D-mal ose, D-
mannose, D- ibose, suc ose, D- ehalose, D-xylose,
D-melezi ose, D- a inose and N-ace yl-D-
glucosamine. S ain SP1PR4T hyd olyzed polysac-
cha ides such as s a ch, pec in, lamina in and
aesculin bu no gela in, cellulose, xylan, lichenan,
sodium algina e, pullulan, chi osan o chi in. En-
zyme ac i i ies o s ain SP1PR4T include
chi obiase, ca alase, acid and alkaline phospha-
ase, leucine a ylamidase, naph hol-AS-B1-
phosphohyd olase, α- and β-galac osidase, α- and
β-glucosidase, β-glucu onidase, N-ace yl-β-
glucosaminidase, α-mannosidase and α- ucosidase
[3,15].
Chemo axonomy
The majo cellula a y acids in T. saanensis
SP1PR4T a e iso-C15:0 (39.9%), C16:1 ω7c (28.4%),
iso-C13:0 (9.8%) and C16:0 (9.8%). The cellula a y
acid composi ions o s ain SP1PR4T we e ela-
i ely simila o ha o T. oseus DSM 18391T, wi h
highe ela i e abundance o iso-C13:0 and a co e-
sponding lowe abundance o iso-C15:0 in s ain
SP1PR4T [3].
Genome sequencing and anno a ion
Genome p ojec his o y
S ain SP1PR4T was selec ed o sequencing in
2009 by he DOE Join Genome Ins i u e (JGI)
communi y sequencing p og am. The Quali y
D a (QD) assembly and anno a ion we e com-
ple ed on Augus 6, 2010. The comple e genome
was made a ailable on Jan 24, 2011. The genome
p ojec is deposi ed in he Genomes On-Line Da a-
base (GOLD) [25] and he comple e genome se-
quence o s ain SP1PR4T is deposi ed in GenBank.
Table 2 p esen s he p ojec in o ma ion and i s
associa ion wi h MIGS e sion 2.0 [16].
Rawa e al.
h p://s anda dsingenomics.o g 61
Figu e 1. Phylogene ic ee highligh ing he posi ion o T. saanensis SP1PR4T ela i e o he o he ype
s ains wi hin he amily Acidobac e iaceae. The maximum likelihood ee was in e ed om 1,359
aligned posi ions o he 16S RNA gene sequences and de i ed using MEGA e sion 5 [14]. Boo s ap
alues (exp essed as pe cen ages o 1,000 eplica es) o >50 a e shown a b anch poin s. Ba : 0.02 sub-
s i u ions pe nucleo ide posi ion. The s ains ( ype s ain=T) and hei co esponding GenBank acces-
sion numbe s a e displayed in pa en heses wi h s ain T. saanensis SP1PR4T shown in bold. B yobac e
agg ega us MPL3 (AM162405) was used as ou g oup. T. saanensis SP1PR4T and T. oseus KBS 63T
(DSM 18391) genome sequences ha e been e ealed.
Figu e 2. Elec on mic og aph o cells o T. saanensis s ain
SP1PR4T (ba 0.5 µm).
Te iglobus saanensis ype s ain SP1PR4T
62 S anda ds in Genomic Sciences
Table 1. Classi ica ion and gene al ea u es o T. saanensis SP1PR4T acco ding o he MIGS ecommenda ions [16].
MIGS ID P ope y Te m E idence codes
Domain Bac e ia TAS [17]
Phylum Acidobac e ia TAS [18,19]
Class Acidobac e ia TAS [20]
Classi ica ion O de Acidobac e iales TAS [21,22]
Family Acidobac e iaceae TAS [18,23]
Genus Te iglobus TAS [1]
Species Te iglobus saanensis TAS [3]
Type s ain: SP1PR4T
G am s ain nega i e TAS [3]
Cell shape od TAS [3]
Mo ili y non-mo ile TAS [3]
Spo ula ion non-spo e o ming TAS [3]
Tempe a u e ange 4–30°C TAS [3]
Op imum empe a u e 25°C TAS [3]
pH ange 4.5-7.5 TAS [3]
Op imum pH 6.0 TAS [3]
Salini y no epo ed NAS
MIGS-22 Oxygen equi emen ae obe TAS [3]
Ca bon sou ce
cellobiose, D- uc ose, D-galac ose, D-glucose,
lac ose, D-mal ose, D-mannose, D- ibose, su-
c ose, D- ehalose, D-xylose, D-melezi ose, D-
a inose, s a ch, pec in, lamina in and aesculin
TAS [3]
MIGS-6 Habi a e es ial TAS [3]
MIGS-15 Bio ic ela ionship ee-li ing TAS [3]
MIGS-14 Pa hogenici y non-pa hogen NAS
Biosa e y le el 1 NAS
Isola ion und a soil TAS [3]
MIGS-4 Geog aphic loca ion Saana jeld, A c ic und a, Finland TAS [3]
MIGS-5 Sample collec ion ime 2004-2005 TAS [3]
MIGS-4.1 La i ude 69°01’N, TAS [3]
MIGS-4.2 Longi ude 20°50’E TAS [3]
MIGS-4.3 Dep h no epo ed NAS
MIGS-4.4 Al i ude no epo ed NAS
*E idence codes - IDA: In e ed om Di ec Assay ( i s ime in publica ion); TAS: T aceable Au ho S a emen
(i.e., a di ec epo exis s in he li e a u e); NAS: Non- aceable Au ho S a emen (i.e., no di ec ly obse ed
o he li ing, isola ed sample, bu based on a gene ally accep ed p ope y o he species, o anecdo al e i-
dence). These e idence codes a e om he Gene On ology p ojec [24].
Rawa e al.
h p://s anda dsingenomics.o g 63
Table 2. Genome sequencing p ojec in o ma ion.
MIGS ID
P ope y
Te m
MIGS 31 Finishing quali y Finished
MIGS-28 Lib a ies used Th ee lib a ies, an Illumina GAii sho gun lib a y (GSGY), a
454 Ti anium s anda d lib a y (GSXT, GWTA) and a pai ed
end 454 (GSFP) lib a y
MIGS 29 Sequencing pla o ms 454 Ti anium s anda d, 454 Pai ed End, Illumina
MIGS 31.2 Sequencing co e age 39× (454), 180× (Illumina)
MIGS 30 Assemble s Newble , Vel e , Ph ap
MIGS 32 Gene calling me hod P odigaL, GenePRIMP
Locud Tag AciPR4
INSDC / Re Seq ID CP002467, NC_014963,
GenBank Da e o Release Oc obe 7, 2011
GOLD ID Gc01604
NCBI p ojec ID 48971
MIGS 13 Sou ce ma e ial iden i ie ATCC BAA-1853, DSM 23119
P ojec ele ance En i onmen al, Biogeochemical cycling o ca bon, Bio echno-
logical, GEBA
G ow h condi ions and genomic DNA ex ac ion
S ain SP1PR4T was cul i a ed in R2 medium as
p e iously desc ibed [3]. Genomic DNA (gDNA) o
high sequencing quali y was isola ed using a
modi ied CTAB me hod and e alua ed acco ding
o he Quali y Con ol (QC) guidelines p o ided by
he DOE Join Genome Ins i u e.
Genome sequencing and assembly
The inished genome o T. saanensis SP1PR4T (JGI
ID 4088690) was gene a ed a he DOE Join ge-
nome Ins i u e (JGI) using a combina ion o
Illumina [26] and 454 echnologies [27]. Fo his
genome, an Illumina GAii sho gun lib a y which
gene a ed 23,685,130 eads o aling 916 Mb, a 454
Ti anium s anda d lib a y which gene a ed
409,633 eads and a pai ed end 454 lib a y wi h an
a e age inse size o 10.8 kb which gene a ed
180,451 eads o aling 157 Mb o 454 da a, we e
cons uc ed and sequenced. All gene al aspec s o
lib a y cons uc ion and sequencing pe o med a
he JGI can be ound a he JGI websi e [28]. The
454 Ti anium s anda d da a and he 454 pai ed
end da a we e assembled oge he wi h Newble ,
e sion 2.3. Illumina sequencing da a was assem-
bled wi h Vel e , e sion 0.7.63 [29]. We in eg a ed
he 454 Newble consensus sh eds, he Illumina
Vel e consensus sh eds and he ead pai s in he
454 pai ed end lib a y using pa allel ph ap, e sion
SPS - 4.24 (High Pe o mance So wa e, LLC). The
so wa e Consed [30,31] was used in he inishing
p ocess. Illumina da a was used o co ec po en ial
base e o s and inc ease consensus quali y using
he so wa e Polishe de eloped a JGI (Alla
Lapidus, unpublished). Possible mis-assemblies
we e co ec ed using gapResolu ion (Cli Han, un-
published), Dup inishe [32], o sequencing cloned
b idging PCR agmen s wi h sub-cloning. Gaps be-
ween con igs we e closed by edi ing in Consed, by
PCR and by Bubble PCR (J-F Cheng, unpublished)
p ime walks. The inal assembly is based on 157
Mb o 454 da a which p o ides an a e age 39×
co e age and 916 Mb o Illumina da a which p o-
ides an a e age 180× co e age o he genome.
Genome anno a ion
Genes we e iden i ied using P odigal [33] as pa
o he Oak Ridge Na ional Labo a o y genome an-
no a ion pipeline, ollowed by a ound o manual
cu a ion using he JGI GenePRIMP pipeline [34].
The p edic ed CDSs we e ansla ed and used o
sea ch he Na ional Cen e o Bio echnology In-
o ma ion (NCBI) non- edundan da abase,
UniP o , TIGRFam, P am, PRIAM, KEGG, (COGs)
[35,36], and In e P o. These da a sou ces we e
combined o asse a p oduc desc ip ion o each
p edic ed p o ein. Non-coding genes and miscel-
laneous ea u es we e p edic ed using RNAscan-
SE [37], RNAMMe [38], R am [39], TMHMM [40],
and signalP [41]. Addi ional gene p edic ion anal-
ysis and unc ional anno a ion we e pe o med
wi hin he In eg a ed Mic obial Genomes Expe
Re iew (IMG-ER) pla o m [42].

Te iglobus saanensis ype s ain SP1PR4T
64 S anda ds in Genomic Sciences
Genome p ope ies
The genome consis s o one ci cula ch omosome
o 5,095,226 bp in size wi h a GC con en o 57.3%
and consis s o 54 RNA genes (Figu e 3, Table 3).
O he 4,333 p edic ed genes, 4,279 a e p o ein-
coding genes (CDSs) and 99 a e pseudogenes. O
he o al CDSs, 67% ep esen COG unc ional ca -
ego ies and 43% consis o signal pep ides. The
dis ibu ion o genes in o COG unc ional ca ego-
ies is p esen ed in Figu e 3 and Table 4.
Discussion
Genome analysis o T. saanensis iden i ied a high
abundance o genes assigned o COG unc ional ca e-
go ies o anspo and me abolism ca bohyd a es
(9.5%) and amino acids (7.6%), ene gy con e sion
(6.2%), cell en elope biogenesis (9.6%) and an-
sc ip ion (9.2%) [15]. This indica es ha he T.
saanensis genome encodes o unc ions in ol ed in
anspo and u iliza ion o nu ien s, mainly ca bo-
hyd a es and amino acids o ene gy p oduc ion and
cell biogenesis o main ain cell in eg i y in cold un-
d a soils. Fu he genome analysis e ealed an
abundance o gene modules o glycoside hyd olas-
es, glycosyl ans e ases, polysaccha ide lyases, ca -
bohyd a e es e ases, and non-ca aly ic ca bohy-
d a e-binding modules wi hin he ca bohyd a e-
ac i e enzymes (CAZy [43]) amily in ol ed in
b eakdown, u iliza ion and biosyn hesis o ca bohy-
d a es [15]. T. saanensis hyd olyzed complex ca bon
polyme s, including pec in, lamina in, and s a ch,
and u ilized suga s such as cellobiose, D-mannose,
D-xylose, D- ehalose and lamina in. This pa allels
genome p edic ions o CDSs encoding o enzymes
such as pec inases, chi inases, algina e lyases,
ehalase and amylases. T. saanensis was unable o
hyd olyze ca boxyme hyl cellulose (CMC) on pla e
assays and lacked CDSs encoding o cellulases in-
ol ed in cellulose hyd olysis. Howe e , he T.
saanensis genome con ained a BcsZ gene encoding
o an endocellulase (GH8) as pa o a bac e ial cel-
lulose syn hesis (bcs) ope on in ol ed in cellulose
biosyn hesis in se e al species. This ope on consis s
o clus e s o genes in close p oximi y o he BcsZ
gene which includes a cellulose syn hase gene
(bcsAB), a cellulose syn hase ope on p o ein (bcsC)
and a cellulose syn hase ope on p o ein (yhj) [15]. In
addi ion, he T. saanensis genome encoded o a
la ge numbe o gene modules ep esen ing glycosyl
ans e ases (GTs) in ol ed in ca bohyd a e biosyn-
hesis which include cellulose syn hase (UDP-
o ming), α- ehalose phospha e syn hase [UDP-
o ming], s a ch glucosyl ans e ase, ce amide β-
glucosyl ans e ase in ol ed in biosyn hesis o cellu-
lose, ehalose, s a ch, hopanoid, and capsula / ee
exopolysaccha ide (EPS) [15]. This sugges s ha T.
saanensis is in ol ed in hyd olysis o lignocellulosic
soil o ganic ma e , u iliza ion o s o ed ca bohy-
d a es and biosyn hesis o exopolysaccha ides.
The e o e, we su mise ha T. saanensis may be cen-
al o ca bon cycling p ocesses in A c ic and bo eal
soil ecosys ems.
Table 3. Genome s a is ics
A ibu e
Value % o To al
Genome size (bp) 5,095,226 100%
DNA coding (bp) 4,578,206 89.9%
DNA G+C (bp) 2,921,371 57.3%
Numbe o eplicons 1 100%
To al genes 4,334 100%
RNA genes 54 1.3%
RNA ope ons 1 -
P o ein coding genes 4,180 98.8%
Pseudo genes 99 2.3%
Genes wi h unc ion p edic ion 3,203 73.9%
Genes in pa alog clus e s 2,220 51.2%
Genes assigned o COGs 3,170 73.2%
Genes wi h P am domains 3,108 71.7%
Genes wi h signal pep ides 1,867 43.1%
Genes wi h ansmemb ane helices 1,082 25%
CRISPR epea s 0 -
Rawa e al.
h p://s anda dsingenomics.o g 65
Figu e 3. G aphical ep esen a ion o ci cula map o he ch omosome o T. saanensis s ain SP1PR4T displaying el-
e an genome ea u es. F om ou side o cen e : Genes on o wa d s and (colo by COG ca ego ies), genes on e-
e se s and (colo by COG ca ego ies), RNA genes ( RNAs g een, RNAs ed, o he RNAs black), GC con en , GC
skew.
Te iglobus saanensis ype s ain SP1PR4T
66 S anda ds in Genomic Sciences
Table 4. Numbe o genes associa ed wi h gene al COG unc ional ca ego ies.
Code Value %age Desc ip ion
J 163.0 4.6 T ansla ion, ibosomal s uc u e and biogenesis
A 2.0 0.1 RNA p ocessing and modi ica in
K 293.0 8.3 T ansc ip ion
L 142.0 4.0 Replica ion, ecombina ion and epai
B 0.0 0.0 Ch oma in s uc u e and dynamics
D 24.0 0.7 Cell cycle con ol, Cell di ision, ch omosome pa i ioning
Y 0.0 0.0 Nuclea s uc u e
V 98.0 2.8 De ense mechanisms
T 174.0 4.9 Signal ansduc ion mechanisms
M 307.0 8.7 Cell wall/memb ane biogenesis
N 56.0 1.6 Cell mo ili y
Z 2.0 0.1 Cy oskele on
W 0.0 0.0 Ex acellula s uc u es
U 113.0 3.2 In acellula a icking and sec e ion
O 122.0 3.4 Pos ansla ional modi ica ion, p o ein u no e , chape ones
C 196.0 5.5 Ene gy p oduc ion and con e sion
G 303.0 8.6 Ca bohyd a e anspo and me abolism
E 243.0 6.9 Amino acid anspo and me abolism
F 69.0 2.0 Nucleo ide anspo and me abolism
H 134.0 3.8 Coenzyme anspo and me abolism
I 116.0 3.3 Lipid anspo and me abolism
P 134.0 3.8 Ino ganic ion anspo and me abolism
Q 85.0 2.4 Seconda y me aboli es biosyn hesis, anspo and ca abolism
R 443.0 12.5 Gene al unc ion p edic ion only
S 323.0 9.1 Func ion unknown
-
1163.
0 26.8 No in COGs
Acknowledgemen s
The wo k conduc ed by he US Depa men o Ene gy
Join Genome Ins i u e is suppo ed by he O ice o
Science o he US Depa men o Ene gy Unde Con ac
No. DE-AC02-05CH11231. This wo k was unded in
pa by he Academy o Finland and he New Je sey
Ag icul u al Expe imen S a ion.
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