1
Supplementary Information to:
2
Adaptation of an abundant Roseobacter RCA organism to pelagic systems revealed by
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genomic and transcriptomic analyses
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Sonja Voget 1, Bernd Wemheuer 1, Thorsten Brinkhoff 2, John Vollmers 1, Sascha Dietrich1, Helge-
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A. Giebel 2, Christine Beardsley 2, Carla Sardemann 2, Insa Bakenhus 2, Sara Billerbeck 2, Rolf
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Daniel 1, Meinhard Simon 2 *
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1
Institute of Microbiology & Genetics, Genomic & Applied Microbiology and Göttingen Genomics
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Laboratory, University of Göttingen, D-37077 Göttingen, Germany.
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26111 Oldenburg, Germany.
Institute for Chemistry and Biology of the Marine Environment, University of Oldenburg, D-
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* corresponding author. m.simon@icbm.de
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Supplementary information includes 4 Figures with the circular representation of the genome of
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Planktomarina temperata RCA23 (S1), the flagellar genes (S2), the photosynthesis gene cluster of
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P. temperata RCA23 and other organisms affiliated to the Roseobacter clade (S3), expression
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patterns of the photosynthesis gene cluster of P. temperata RCA23 during day and night during a
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phytoplankton spring bloom in the North Sea (S4) and 7 Tables with genomic and metagenomic
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data on this organism and others of the Roseobacter clade. For Tables S4, S6 and S7 see extra files.
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Figure legends
Figure S1: Circular representation of the genome of Planktomarina temperata RCA23. From the
outer to the innermost circle: 1. Genomic islands (GIs, red). 2 and 3: Leading and lagging strand
colored according to the assigned Clusters of Orthologous Groups (COG) categories. 4:
transposases/integrases (red), rRNA genes (purple). 5: tRNAs. 6-22: Homologs to genes in 17
organisms of the Roseobacter clade as listed in Table S3, colored according to subclades like in Fig.
1. ORFs of P. temperata were determined by reciprocal BLAST-analysis with global alignments
(see Methods) against the proteome datasets of the 17 organisms. Query organisms:
Rhodobacterales bacterium HTCC2150, Maritimibacter alkaliphilus HTCC2654, Jannaschia sp.
CCS1, Dinoroseobacter shibae DFL12, Loktanella vestfoldensis SKA53, Octadecabacter
antarcticus 307, Octadecabacter arcticus 238, Roseovarius sp. TM1035, Roseovarius sp. 217,
Sagittula stellata E-37, Oceanicola batsensis HTCC2597, Sulfitobacter NAS-14.1, Sulfitobacter sp.
GAI101, Roseobacter litoralis Och149, Rhodobacterales bacterium HTCC2083, Phaeobacter
inhibens DSM17395, Ruegeria pomeroyi DSS-3. 23: G+C-content of the chromosome of P.
temperata with violet areas below average and olive areas above average.
Figure S2 Neighbor-joining phylogeny of flagellar gene sets in Roseobacter clade members
(marked in red) and related gene sets in other Alpha- and Gammaproteobacteria based on
concatenated protein sequences. The subtree containing flagellar protein sequences of
Gammaproteobacteria was collapsed. Bootstrap values are given for major nodes. The resulting
phylogenetic tree shows that the flagellar gene sets of the Roseobacter clade are divided into two
distinct groups (group I and II) which are more closely related to gene sets of Gammaproteobacteria
than to each other. The flagellar genes of P. temperata (marked in bold) fall into group II which
contains relatively few sequences of Roseobacter clade members but includes strains of the
SAR116 clade (Cand. Puniceispirillum marinum IMCC1322, Alphaproteobacterium HIMB 100)
and of Rhodobacter sphaeroides. In contrast, the majority of flagella gene sets in the Roseobacter
clade belong to group I.
For the phylogenetic relationship of the flagellar gene sets, genes belonging to the flagellar cluster
were identified in the genomes of 38 Roseobacter clade members based on existing annotations and
on reciprocal BLASTp analyses. Related gene sets from other bacterial taxa (displayed in black)
were obtained by BLASTp analyses of the NCBI nt database using multiple flagellar proteins as
query. When multiple flagellar gene sets were present in the same genome, numbers were assigned
to the individual sets (indicated by square parentheses). For each gene set, alignments of 15 shared
flagellar proteins (FlgA, FlgB, FlgC, FlgD, FlgF, FlgG, FlgH, FlgI, FlhA, FlhB, FliE, FliI, FliL,
FliQ, and FliR) were produced using clustalW v1.83. The alignments were concatenated and
imported into ARB v5.1 where a filter was created to remove gapped sites and the remaining 3,673
alignment positions per concatenated sequence were subjected to neighbor-joining analysis.
Figure S3 Photosynthesis gene cluster (PGC) of P. temperata RCA23, a BAC clone and other
organisms affiliated to the Roseobacter clade. Shown is the different organization of the PGC of
members of the Roseobacter clade and environmental clone BAC-60D04 (NCBI Accession
AE008921) derived from Californian coastal waters (Béjà et al., 2002). Homologous regions are
indicated by blue shaded vertical areas and black lines, respectively. Re-arrangements are marked
by red shaded areas. Genes are colored according to biological categories: green,
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bacteriochlorophyll biosynthesis (bch); orange, carotenoid biosynthesis (crt); red, light harvesting
and photosynthesis reaction center (puf); blue, cytochrome c2; grey, accessory genes.
Figure S4 Transporter proteins of P. temperata RCA23 in comparison to those of other organisms
of the Roseobacter clade. Relation between total numbers of transporters and ABC transporters (A).
Box-Whisker plot of ABC transporters (B), ABC-/total transporters (C) and TRAP transporters (D)
of 14 members of the Roseobacter clade associated to other organisms, surfaces or sediment and of
24 members with a pelagic life style listed in supplementary Table S2. Data include 12 closed and
26 draft genomes. Blue circle and +: P. temperata RCA23. The boxes show the median (solid line),
mean (dashed line), the 25th and 75th percentile and the whiskers the 10th and 90th percentiles. :
outlayers. For further details see supplementary Tables S2 and S3.
Figure S5 Expression patterns of the photosynthesis gene cluster of P. temperata RCA23 at station
13 during day and station 9 at night during a phytoplankton spring bloom in the southern North Sea
in May 2010. Genes are colored according to biological categories: green, bacteriochlorophyll
biosynthesis (bch); orange, carotenoid biosynthesis (crt); red, light harvesting and photosynthesis
reaction center (puf).
Figure S6 Representation of the genome of Planktomarina temperata RCA23 in metagenomic data
sets of the north-western Atlantic Ocean. (A) Overview of the stations visited by the Global Ocean
Sampling (GOS) expedition in the western coastal Atlantic Ocean (Rusch et al., 2007). (B) Salinity,
temperature, chlorophyll and mapped reads (bar) of the genome of P. temperata RCA23 at the
stations shown above.
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Table S1. Overview of metagenomic and metatranscriptomic datasets used in this study.
Data sets used in this
study
type
Sequencing
technology
Raw-reads
No. of reads
(trimmed,
rRNA free)
Reference
DNA
Illumina
24 331 052
23 381 812
This study
RNA
Illumina
24 879 579
2 223 804
DNA
Illumina
13 125 978
12 671 944
RNA
Illumina
26 176 832
8 101 537
DNA
Illumina
16 877 252
16 156 091
RNA
Illumina
26 985 711
15 349 574
northwestern Atlantic
(stations GOS02-13)
DNA
Sanger
1 083 836
-
Norwegian fjord
DNA
454
863 687
-
RNA
454
256 537
-
Station 3, non-bloom
Station 9, bloom-night
Station 13, bloom-day
308
309
310
311
312
313
314
315
This study
This study
Rusch et al.
Gilbert et al
Rusch DB, et al. (2007). The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic
through eastern tropical Pacific. PLoS Biology 5:e77.
Gilbert JA, et al. (2008). Detection of large numbers of novel sequences in the metatranscriptomes
of complex marine microbial communities. PLoS One 3:e3042.
10
Table S2. Overview of genome characteristics and general genome comparisons of organisms of the Roseobacter clade isolated from
associations (assoc) with various organisms, surfaces or sediment and from pelagic environments and ordered according to genome size. For
comparison respective data of Cand. Pelagibacter ubique HTCC1062 are also given. The number of plasmids was derived from plasmid
replication systems. Data were taken from the Integrated Microbial Genomes and Metagenomes (IMG; http://img.jgi.doe.gov/) platform.
F: finished genomes; D: draft genomes. nd: not determined.
CDS: Coding DNA sequences; COG: Cluster of orthologous groups; ABC: ATP-binding cassette;
TRAP: Tripartite ATP-independent periplasmic.
Status
F
F
F
F
D
F
F
F
D
F
D
F
F
F
D
Genome Name
Cand. Pelagibacter
ubique HTCC1062
Nautella italica R11
Ruegeria sp.
TM1040
Phaeobacter
inhibens 2.10
Roseovarius sp.
TM1035
Phaeobacter
inhibens DSM17395
Roseobacter
denitrificans OCh
114
Dinoroseobacter
shibae DFL-12,
DSM 16493
Ruegeria sp. KLH11
Ruegeria pomeroyi
DSS-3
Silicibacter sp.
TrichCH4B
Roseobacter litoralis
Och 149
Octadecabacter
antarcticus 307
Octadecabacter
arcticus 238
Citreicella sp. SE45
type
Scaf
fold
Cou
nt
GC
geno
me
size
%
codi
ng
Gene
Count
CDS
Count
COG
Homolog
CDSs
(alignment
min. 30%
and e-value
<1e-20)
trans-port
proteins
ABC-type
transport
proteins
TRAP
-type
trans
port
protei
ns
amino
acid
transpo
rt
proteins
Plasmids
total
%
Mb
%
total
total
%
total
%
total
per Mb
total
per Mb
total
total
total
pelagic
1
30
1.31
96.1
1 394
1 354
81.13
847
27.7
95
73
67
51.1
9
31
0
assoc
2
60
3.82
88.7
3 725
3 656
1 860
60.9
321
84
256
67.0
27
63
1
assoc
3
60
4.15
89.0
3 964
3 870
75.45
1 825
59.7
375
90
289
69.6
42
51
4
assoc
4
60
4.16
88.0
3 798
3 729
82.52
1 894
62.0
371
89
289
69.5
27
74
3
assoc
15
61
4.21
91.1
4 158
4 102
73.42
1 847
60.4
380
90
275
65.3
53
100
1
assoc
4
60
4.23
88.8
3 960
3 891
80.03
1 891
61.9
369
87
297
70.2
22
69
3
assoc
5
59
4.33
89.4
4 201
4 146
73.22
1 923
62.9
432
100
324
74.8
64
72
4
assoc
6
66
4.42
89.9
4 271
4 219
74.29
1 861
60.9
407
92
273
61.8
78
55
5
assoc
6
58
4.49
86.4
4 338
4 274
68.88
1 797
58.8
327
73
241
53.7
34
51
2
assoc
2
64
4.60
90.0
4 355
4 283
78.05
1 941
63.5
447
97
321
69.8
72
114
1
assoc
8
59
4.69
89.1
4 814
4 735
68.92
1 821
59.6
461
98
348
74.2
55
45
nd
assoc
4
57
4.74
89.1
4 577
4 537
77.91
1 982
64.9
509
107
387
81.6
66
95
3
assoc
18
55
4.91
83.4
5 544
5 495
58.75
1 906
62.4
428
87
339
69.0
48
58
1
assoc
8
55
5.39
81.8
5 883
5 834
60.58
1 888
61.8
395
73
305
56.6
50
80
2
assoc
9
67
5.52
87.9
5 499
5 427
71.65
1 721
56.3
644
117
443
80.3
132
103
3
11
Status
D
D
F
D
D
D
D
D
D
D
D
D
D
D
F
D
D
D
Genome Name
Rhodobacterales
sp.HTCC2255
Loktanella
vestfoldensis SKA53
Planktomarina
temperata RCA23
Loktanella sp. CCS2
Thalassiobium sp.
R2A62
Ruegeriar
lacuscaerulensis ITI1157
Sulfitobacter sp. EE36
Rhodobacterales sp.
HTCC2150
Roseovarius
nubinhibens ISM
Sulfitobacter sp.
NAS-14.1
Rhodobacterales sp.
HTCC2083
Oceanicola
granulosus
HTCC2516
Oceanibulbus
indolifex HEL-45
Roseobacter sp.
AzwK-3b
Jannaschia sp.
CCS1
Rhodobacterales sp.
Y4I
Oceanicola batsensis
HTCC2597
Maritimibacter
alkaliphilus
HTCC2654
type
Scaf
fold
Cou
nt
GC
geno
me
size
%
codi
ng
Gene
Count
CDS
Count
COG
Homolog
CDSs
(alignment
min. 30%
and e-value
<1e-20)
trans-port
proteins
ABC-type
transport
proteins
TRAP
-type
trans
port
protei
ns
amino
acid
transpo
rt
proteins
Plasmids
total
%
Mb
%
total
total
%
total
%
total
per Mb
total
per Mb
total
total
total
pelagic
12
37
2.54
92.7
2 240
2 177
87.46
1 565
51,2
247
111
179
47.6
38
54
0
pelagic
14
60
3.06
91.9
3 117
3 068
75.01
1 843
60.3
272
89
205
67.0
34
45
0
pelagic
1
54
3.29
89.8
3 101
3 056
83.23
/
/
287
87
208
63.2
43
53
0
pelagic
11
55
3.49
92.2
3 703
3 660
69.46
1 841
60.2
300
86
234
67.0
35
46
0
pelagic
1
55
3.49
90.1
3 744
3 696
67.68
1 913
62.6
285
82
221
63.3
31
48
0
pelagic
2
63
3.52
90.9
3 677
3 611
72.97
1 828
59.8
298
85
222
63.1
28
44
1
pelagic
15
60
3.55
91.0
3 542
3 474
76.31
1 764
57.7
333
94
215
60.6
73
54
2
pelagic
25
49
3.58
91.6
3 713
3 667
70.11
1 943
63.6
273
76
186
52.0
53
59
3
pelagic
10
64
3.67
89.8
3 605
3 547
74.84
1 737
56.8
322
88
202
55.0
76
70
1
pelagic
27
60
4.00
90.1
4 026
3 962
73.7
1 788
58.5
348
87
229
57.3
65
53
5
pelagic
5
53
4.02
87.6
4 226
4 179
69.12
2 009
65.7
347
86
255
63.4
66
76
1
pelagic
85
70
4.04
91.5
3 855
3 792
77.12
1 736
56.8
459
114
384
95.0
35
52
2
pelagic
105
60
4.11
89.4
4 208
4 153
73.31
1 780
58.2
411
100
286
69.6
68
79
1
pelagic
31
62
4.18
88.8
4 197
4 145
69.67
1 825
59.7
325
78
229
54.8
59
78
0
pelagic
2
62
4.40
90.8
4 339
4 283
73.17
1 917
62.7
400
91
303
68.9
59
39
1
pelagic
5
64
4.34
86.2
4 206
4 133
73.3
1 782
58.3
317
73
218
50.2
42
73
2
pelagic
23
66
4.44
89.2
4 261
4 212
75.1
1 739
56.9
437
98
293
66.0
82
108
4
pelagic
46
64
4.53
90.1
4 763
4 712
67.86
1 751
57.3
381
84
260
57.4
64
88
3
12
Status
D
D
D
D
D
D
Genome Name
Sulfitobacter sp.
GAI101
Roseobacter sp.
SK209-2-6
Roseobacter sp.
MED193
Roseovarius sp. 217
Sagittula stellata E37
Pelagibaca
bermudensis
HTCC2601
type
Scaf
fold
Cou
nt
GC
geno
me
size
%
codi
ng
Gene
Count
CDS
Count
COG
Homolog
CDSs
(alignment
min. 30%
and e-value
<1e-20)
trans-port
proteins
ABC-type
transport
proteins
TRAP
-type
trans
port
protei
ns
amino
acid
transpo
rt
proteins
Plasmids
total
%
Mb
%
total
total
%
total
%
total
per Mb
total
per Mb
total
total
total
pelagic
9
59
4.53
87.2
4 258
4 203
76.33
1 857
60.8
414
91
291
64.2
74
59
3
pelagic
29
57
4.55
88.8
4 610
4 537
71.13
1 851
60.6
394
87
276
60.7
59
86
3
pelagic
19
57
4.65
89.1
4 605
4 535
71.9
1 901
62.2
395
85
281
60.4
51
80
2
pelagic
37
61
4.76
90.2
4 823
4 772
72.53
1 842
60.3
417
88
277
58.2
73
100
2
pelagic
39
65
5.26
88.3
5 121
5 067
72.66
1 908
62.4
546
104
399
75.9
90
89
3
pelagic
103
66
5.42
88.6
5 519
5 452
70.95
1 830
59.9
596
110
408
75.3
116
87
3
13
Table S3. Mean values+standard deviation of genomic features and COG categories indicated of the members of the
Roseobacter clade associated to other organisms, surfaces and sediment and with a pelagic life style listed in supplementary
Table S4, Planktomarina temperata RCA23 and of Photobacterium angustum and Sphingopyxis alaskensis. *: significantly
different means as tested by Student’s t-test (P<0.03; genome size, % coding genes, ABC/total transporters, COG V) or Mann
Whitney Rank Sum test (P<0.015; ABC transporters, COG I). N: number of organism of the subgroup; CDS: Coding DNA
Sequences. Data of P. angustum and S. alaskensis are from Lauro et al. (2009) and the Integrated Microbial Genomes and
Metagenomes (IMG; http://img.jgi.doe.gov/) platform.
Feature
Associated
Pelagic
N
14
24
GC content (%)
60.07+3.58
59.28+6.82
Genome size (Mb)
4 547+478
4 059+681 *
% coding genes
88.05+2.57
89.82+1.62 *
CDS
4 442.7+689.2 4 003.9+699.8
Transporter proteins
419.0+82.5
366.8+86.0
ABC transporters
313.4+53.6
260.9+63.5 *
ABC/total
0.75+0.04
0.71+0.05 *
ABC/Mb
68.8+7.9
63.2+9.8
TRAP transporters
55.0+28.1
58.9+21.3
COG N (cell motility; %)
1.53+0.44
1.22+0.54
COG K (transcription; %)
8.03+1.01
7.53+0.99
COG V (defense; %)
1.37+0.20
1.14+0.18 *
COG T (signal transduction ; %)
4.45+0.79
4.16+0.85
COG I (lipid transport and metabolism; %)
4.58+0.47
5.34+0.86 *
COG Q (secondary metabolites, biosynthesis,
3.52+0.44
3.87+0.65
transport and catabolism, %)
P. temperata
P. angustum
S. alaskensis
1
54
3.29
89.75
3 056
287
208
0.72
63.2
43
1.71
6.15
1.01
2.72
6.18
4.63
1
39.69
5.10
85.19
4 558
293
182
0.62
36.7
4
3.31
7.53
1.47
7.07
2.96
2.17
1
65.46
3.37
90.63
3 208
116
50
0.43
14.9
0
1.01
6.62
1.24
3.63
4.41
3.54
14
Table S4. Complete CDS list of P. temperata RCA23 and combined results of the reciprocal blast comparisons against 39
Roseobacter genomes. Orthologous genes with an e-value of the corresponding blast hit <1e-20 and min. global alignment of
30% are colored.
See extra file!
15
Table S5. Percent of COG categories N (cell motility), K (transcription), V (defense), T (signal transduction), I (lipid transport
and metabolism) and Q (secondary metabolites, biosynthesis, transport and catabolism) of organisms of the Roseobacter clade
isolated from associations with various organisms, surfaces or sediment and from pelagic environments. For comparison
respective data of Cand. Pelagibacter ubique are also given. Data were taken from the Integrated Microbial Genomes and
Metagenomes (IMG; http://img.jgi.doe.gov/) platform.
Genome Name
Associated
Dinoroseobacter shibae DFL-12, DSM 16493
Nautella italica R11
Octadecabacter antarcticus 307
Octadecabacter arcticus 238, DSM 13978
Phaeobacter inhibens 2.10
Phaeobacter inhibens DSM 17395
Roseobacter denitrificans OCh 114
Roseobacter litoralis Och 149
Ruegeria pomeroyi DSS-3
Ruegeria sp. TM1040
Citreicella sp. SE45
Roseovarius sp. TM1035
Ruegeria sp. KLH11
Ruegeria sp. TrichCH4B
N
K
V
T
I
Q
%
%
%
%
%
%
1.14
1.82
1.32
1.21
1.69
1.64
1.43
1.35
0.85
2.17
1.27
2.46
1.17
1.90
6.86
8.07
7.11
6.25
8.62
8.30
7.15
7.63
9.89
9.29
8.60
7.73
7.97
9.07
1.26
1.46
1.23
0.83
1.40
1.33
1.72
1.40
1.44
1.34
1.37
1.51
1.54
1.33
3.89
5.17
3.51
2.90
4.98
4.67
4.52
4.37
4.15
6.08
4.19
4.59
4.05
5.21
4.37
4.68
4.71
3.60
4.75
4.86
4.52
4.21
5.74
4.61
4.29
4.65
4.75
4.31
3.65
3.39
3.45
2.63
3.73
3.63
3.38
3.56
4.50
3.28
3.86
3.93
3.38
2.95
16
Pelagic
Planktomarina temperata RCA23
Jannaschia sp. CCS1
Loktanella sp. CCS2
Loktanella vestfoldensis SKA53
Maritimibacter alkaliphilus HTCC2654
Oceanibulbus indolifex HEL-45
Oceanicola batsensis HTCC2597
Oceanicola granulosus HTCC2516
Pelagibaca bermudensis HTCC2601
Rhodobacterales bacterium HTCC2083
Rhodobacterales bacterium HTCC2150
Rhodobacterales bacterium Y4I
Rhodobacterales bacterium HTCC2255
Roseobacter sp. AzwK-3b
Roseobacter sp. MED193
Roseobacter sp. SK209-2-6
Roseovarius nubinhibens ISM
Roseovarius sp. 217
Sagittula stellata E-37
Ruegeria lacuscaerulensis ITI-1157
Sulfitobacter sp. EE-36
Sulfitobacter sp. GAI101
Sulfitobacter sp. NAS-14.1
Thalassiobium sp. R2A62
N
K
V
T
I
Q
1.71
1.32
1.17
1.97
0.53
1.04
1.13
2.25
1.86
1.64
0.31
1.78
0.21
0.75
0.97
1.62
0.26
1.17
1.45
1.16
1.33
1.51
1.01
1.10
6.15
8.31
7.23
6.46
7.74
7.52
7.06
7.27
7.99
6.95
6.80
8.27
5.80
6.94
9.21
10.09
8.67
8.66
7.87
7.38
7.33
6.68
7.48
6.91
1.01
0.94
1.17
1.20
0.93
0.91
1.03
1.21
1.02
1.06
1.23
1.39
0.93
1.57
1.27
1.04
0.93
1.03
1.10
1.30
1.26
1.45
1.15
1.26
2.72
4.19
4.04
4.15
4.02
5.38
3.47
3.77
4.16
2.91
3.73
6.23
2.48
4.58
4.92
5.15
3.82
4.43
4.97
4.21
4.00
4.86
3.81
3.75
6.18
5.01
4.94
5.09
6.96
4.93
8.00
4.57
4.75
5.92
5.38
4.57
4.35
4.75
5.83
4.79
5.00
5.32
5.29
5.03
6.10
5.97
4.95
4.38
4.63
4.03
2.92
3.55
4.36
3.57
4.94
3.80
3.80
4.62
4.80
3.60
2.69
3.08
4.08
3.54
4.04
3.72
4.27
3.24
4.14
4.95
3.67
2.88
17
1
2
3
4
5
6
7
8
9
10
11
Table S6. Normalized read counts (NPKM) of the transcripts at stations 9 (bloom, night) and 13 (bloom, day) and differences
between night and day
See extra file!
Table S7 Coverage of P. temperata RC23 genes from combined stations GS012-13 of the GOS data set and the Norwegian fjord
metagenome.
See extra file!
12
18