Phylogenetic analysis of a novel sulfate

PEMS Microbiology
Letters 126 (1995) 277-282
Phylogenetic analysis of a novel sulfate-reducing magnetic
bacterium, RS-1, demonstrates its membership of the
S-Proteobacteria
Ryuji Kawaguchi b, J. Grant Burgess a, Toshifumi Sakaguchi a, Haruko Takeyama a,
Richard H. Thornhill a, Tadashi Matsunaga a9*
aDepartment of Biotechnology, Tokyo Uniuersily ofAgriculture and Technology, 2-24-16 Naka-cho, Koganei-shi, Tokyo 184, Japan
b Center for Molecular Biology and Cytogenetics,
Received 25 October 1994; revised 30 December
SRL.., Hachioji, Tokyo 192, Japan
1994; accepted 3 January 1995
Abstract
Most of the 16s ribosomal RNA gene of a sulfate-reducing magnetic bacterium, RS-1, was sequenced, and phylogenetic
analysis was carried out. The results suggest that RS-1 is a member of the GProteobacteria, and it appears to represent a new
genus. RS-1 is the first bacterium reported outside the cw-Proteobacteria that contains magnetite inclusions. RS-1 therefore
disrupts the correlation between the a-Proteobacteria and possession of magnetite inclusions, and that between the
GProteobacteria and possession of greigite inclusions. The existence of RS-1 also suggests that intracellular magnetite
biomineralization is of multiple evolutionary origins.
Keywords:
16s ribosomal RNA, Sulfate-reducing magnetic bacteria; Evolution of magnetite biomineralization;
Bean-shaped magnetic inclusions; SProteobacteria; Magnetic bacteria
1. Introduction
Magnetic bacteria contain ferromagnetic
crystalline inclusions which cause the cells to orient and
swim in the direction of an external magnetic field
[l]. Magnetic bacteria make an important contribution to the global iron cycle [2]; are probably the
main source of stable remanent magnetism in marine
sediments [3]; and have numerous potential biotechnological applications [4]. The biological function of
bacterial magnetic inclusions is still unknown, al-
* Corresponding
author.
Fax: + 81 (423) 857 713
Tel.:
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(423) 814 221 ext. 375;
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SSDI 0378-1097(95)00023-2
of European
Microbiological
RS-1;
though it has been suggested that they have a navigational function [5-71. Various types of magnetic
bacteria are known, including cocci [8], spirilla [9],
vibrios [lo], ovoid bacteria [ll], rod-shaped bacteria
1121,and multicellular bacteria [13].
Bacterial magnetic inclusions are composed of
either magnetite (Fe,O,) [14] or greigite (Fe,S,)
[15,16]. Bacteria containing greigite inclusions are
members of the GProteobacteria [17]. Previously
reported bacteria containing magnetite inclusions
were members of the cu-Proteobacteria [18,19]. Bacteria containing magnetite inclusions include cocci,
spirilla, and vibrios, and each of these morphological
types forms a distinct phylogenetic group [17]. However, these groups are all moderately related, and it
Societies. All rights reserved
R. Kawaguchi
278
et ul. / FEMS Microbiology
was therefore uncertain whether intracellular magnetite biomineralization
had evolved separately for
each morphological type.
A novel magnetic bacterium containing magnetite
inclusions, RS-1, was recently discovered [20]. RS-1
is helicoid to rod-shaped, and therefore did not appear to be a member of the magnetic cocci, spirilla
or vibrio groups within the cr-Proteobacteria. RS-1
magnetic inclusions are bean-shaped, whereas other
magnetite inclusions are rectangular.
Furthermore,
RS-1 is the only known dissimilatory sulfate-reducing magnetic bacterium. In this work, in order to
assess whether the unusual physiology, morphology
and crystallography
of RS-1 reflected its phylogenetic position, most of the 16s rRNA gene (16s
rDNA) was sequenced, and compared with those of
other bacteria.
2. Materials and methods
2.1. RS-1 DNA extraction and primer design
RS-1 was cultured as described previously [20].
Genomic DNA was extracted using a standard protocol [21]. Primers which will anneal to the 16s rDNA
of almost all proteobacteria were designed by comparing 16s rRNA sequences from representative
members of the IX-, /3-, y-, and S-Proteobacteria.
The forward primer was S-AGAGTFTGATCATGGCTC3’ (E. coli positions 8-25), and the reverse
primer was 5’-TAAGGAGGTGATCCAACCGC-3’
(E. coli positions 1523-1542). These were expected
to amplify approximately 1500 bp of 16s rDNA.
2.2. rDNA amplification
and sequencing
The polymerase chain reaction (PCR) was carried
out in a reaction containing 2.5 U of AmpliTaq DNA
polymerase (Perkin Elmer Cetus, Norfolk, USA), 20
nmol of each dNTP, 10 ~1 of 10 X PCR buffer
(Perkin Elmer Cetus), 10 pmol of each primer, and
0.1 g of template DNA. The reaction volume was
made up to 100 ~1 with sterile distilled water, and
the reaction was overlaid with 50 ~1 of mineral oil.
One PCR cycle consisted of 1 min at 94°C 2 min at
50°C and 3 min at 72°C and this was repeated 35
times, using a thermal cycler (PJ 2000; Perkin Elmer
Letters 126 (1995) 277-282
Cetus). The PCR products were sequenced directly,
using an automatic
sequencer
(373A; Applied
Biosystems/Perkin
Elmer, Foster City, USA), according to the manufacturer’s instructions, using the
same primers as the PCR.
2.3. Phylogenetic
analysis
The 16s rDNA sequence of RS-1 was aligned
with other proteobacterial 16s rDNA sequences, using the Clustal V algorithm [22], and the alignment
was fine-tuned manually. Percentage similarity was
calculated [23], using positions 256-412, 512-526,
and 529-875, which are homologous in all the sequences aligned. Evolutionary distance and an estimation of mutations per nucleotide position were
calculated from percentage
similarity
data by a
method which partially corrects for multiple and
back mutations using information
from conserved
nucleotide positions [24]. Phylogenetic
trees were
constructed from the evolutionary distance data by
the neighbor-joining
method [25].
2.4. GenBank nucleotide
accession numbers
16s rDNA sequences referred to in this work
have the following GenBank and EMBL accession
numbers:
Desulfovibrio
longreachii,
224450; D.
baculatus, M37311; D. salexigens,
M34401; D.
desulfuricans,
M34113;
Pelobacter
propionicus,
X70954;
Desulfobulbus
propionicus,
M34410;
Geobacter metallireducens,
L07834; Magnetobacterium bavaricum,
X71838; MMP1991, L06457;
Magnetospirillum
magnetotacticum,
M58171; Magnetospirillum sp. AMB-1, D17514; MV-1, LP6455;
Pseudomonas
testosteroni,
Ml 1224; Escherichia
coli, VO0348.
3. Results
3.1. Secondary
structure and signature analysis
A 19-bp helix between E. coli positions 184 and
195 in the RS-1 16s rDNA is characteristic of the
GProteobacteria
(Fig. 1). A 21-bp helix between
positions 200 and 217 was also consistent with
placement of RS-1 in the S-Proteobacteria [26]. The
R. Kawaguchi et al. / FEMS Microbiology Letters 126 (1995) 277-282
279
Helix omaistent
171
Hdixchsractcristicof
&,&__
1%
184
withpbcematin
200 ~a_-
217
229
1
Eschrrichto colt
MTACCCCATAACCTC----GCAAGAC----------CAAAGACGCGGACCTTCGGGC--CTC~GCCATCGGAT
RS-1
AATACCGGATACGCTCCAAmCGmG-------GGGG~GGCGGC~CTG~G~GCT~CGTATCTG~T
&sulfovibrio longreachii
AATACCGAATACGCTCCGAmCACA---GTTCGGGGGAAAGGTGGCCTCTGCTTGCAAGCTACCGCTCATGGAT
LIesulfovibriobacul&~
AATACCGGATA-GTCTNGCT~~GTCG-GTAAAGGATGCCTCTG~T--ATGCATTCGTCCGAGGAT
Lksulfovibriosakxigem
AATACCGGATACGmCATAmAACTNNATNA-G-AGAAAGGTGGCCTCTNTTT-CAAGCTATCACTmGGAT
Pelobacter pvpionicus
AATACCTtATAAGCCCACGACCGCmGCTCCTTGCGGGAAAT
Mm1991 (nmglaic bactelilml)
----------------------------TGAATT----AA
Geotnicm metallireducem
AATACCGtATAAGCCCACGtGTCCTTGGATTCTGCGGGAT
a~surfovibriodesul&ricam
AATACCGCATACGCTCAAAATCAACT----mTCAGGAAAGT
Lksulj&bu0usproptonicus
MTACCGGATAAAGTCGAmACACAAGTAGATTGATGAAAGT
Magnetospitillummagneto~ticum
AATACCGCATACGCCC--------------TTCGGGGGAAT
Magnetospirillam sp. AM-1
AATACCGCATACGCCC--------------~CGGGG~M--G------A~AT--------CGCC~~~T
MagnetospiriUumgiyph&aldeme
AATACCGCATACGCCC----
~~~-------~CGGGG~AAA--G-~-~--AmAT--_--______CGCC~~~T
MV-1 (magmtic vilnio)
AATACCGCATACGCCC--------------nCCGGGG~--G------A~AT--------CGCTGTTTGAT
PsewkmwlW t.?stostelWni
AATACCGCATGAGATC--------------TA(GGATGAAG
Magnetokterkm
AATCCCGGATMCACC--------------ACGGATAGCAT
bavartcum
Fig. 1. Section of the 16s rDNA sequence between E. coli positions 171 and 229 from RS-1, related members of the GProteobacteria,
other
magnetic bacteria, and representative members of the 8- and y-Proteobacteria.
Between E. coli positions 184 and 195, RS-1 DNA has a
19-bp helix, which is characteristic of the GProteobacteria
(cf. Geobacter metallireducens and Desulfouibrio desulfuricans sequences). The
helix between E. coli positions 200 and 217 is also consistent with placement in the GProteobacteria.
Desuljbvibrio
longreachii
Desu&n&io desnlfvricnns
Desvlfmibrio bactdatus
RS-1
Desulfovibrio salexigens
Pelobacter propionicuv
b - Roteobacluia
Geobactcr tnetallireducenv
Desulfobulbus propionicus
Erchcrichia coli
-
y - Proteobactetia
Magnetobacterium bavarkum
16.8
I
I
I
I
I
I
I
I
1
16
14
12
10
8
6
4
2
0
Fig. 2. Phylogenetic tree of 16s rDNA from RS-1, related members of the GProteobacteria,
other magnetic bacteria, and representative
and is most closely
members of the p- and yproteobacteria.
RS-1 represents a distinct phylogenetic group within the GProteobacteria,
related to Desulfovibrio spp. and Geobacter metallireducens.
a Values below the diagonal represent percentage
11.8
10.1
11.3
12.2
16.7
11.2
10.8
21.6
14.7
17.6
17.6
17.6
18.0
19.4
16.6
1
10.4
11.9
14.1
8.2
12.4
19.1
14.5
15.8
15.8
16.0
15.4
17.1
14.2
85.4
84.6
a
divergence.
9.9
10.1
13.6
15.5
6.4
12.7
20.0
13.7
17.8
17.8
18.2
15.8
19.8
15.8
86.0
2
3
13.9
17.5
10.9
14.8
19.4
15.4
15.8
15.6
15.2
14.9
19.2
13.3
86.2
87.6
84.2
4
from RS-1, other magnetic
Percent similarity
matrix for 16s rRNA sequences
1. RS-1
2. Desulfovibrio longreachii
3. Desulfovibrio baculatus
4. Desulfouibrio salexigens
5. Pelobacter propionicus
6. Desulfobulbuspropionicus
7. Desulfovibrio desuifuricans
8. Geobacter metallireducens
9. Magnetobacterium bauaricum
10. MMP1991 (magnetic bacterium)
11. Magnetospirillum magnetotacticum
12. Magnetospirillum sp. strain AMB-1
13. Magnetospirillum gryphyiswaldense
14. MV-1 (magnetic vibrio)
15. Pseudomonas testosteroni
16. Escherichia coli
Species
Table 1
Similarity
10.7
13.8
4.8
18.4
11.2
16.0
16.0
15.8
14.8
19.6
14.6
85.4
84.6
83.2
83.2
5
bacteria,
15.7
13.4
20.2
10.7
19.8
19.8
20.0
20.4
20.8
19.6
79.4
82.0
79.8
79.0
86.6
6
13.5
19.2
14.5
16.6
16.6
16.8
16.4
19.6
15.6
86.4
92.6
87.0
86.8
85.0
82.0
7
and representative
18.3
11.1
16.1
16.1
15.7
13.7
18.3
14.5
86.2
84.6
81.6
82.2
93.6
82.8
83.8
8
20.9
21.4
21.6
19.8
19.4
21.4
21.4
75.4
76.6
74.9
76.8
77.0
76.2
77.6
78.0
9
17.9
17.7
18.3
17.7
21.7
17.3
81.0
83.4
78.2
80.2
86.4
85.6
81.8
85.2
73.2
10
0.2
5.2
11.6
17.6
15.4
80.0
80.0
79.0
81.8
82.0
76.8
80.8
81.2
74.5
78.0
11
members of the proteobacterial
5.4
11.6
17.6
15.2
80.0
80.0
79.4
82.0
82.0
76.8
80.8
81.2
74.5
78.0
99.6
12
11.6
16.8
14.4
79.8
78.8
79.0
82.6
81.2
76.8
80.0
81.4
75.8
77.2
94.2
94.0
13
subdivision
14
19.4
16.2
79.6
81.8
80.2
82.6
82.0
75.8
81.0
83.4
76.6
78.4
86.8
86.8
86.2
15
15.6
76.4
76.8
77.2
77.4
77.2
75.6
76.2
78.4
76.0
74.0
79.8
79.8
80.8
77.0
16
81.2
82.2
81.4
84.2
83.4
76.6
81.6
83.0
76.0
78.8
83.6
83.8
83.4
81.2
82.6
R. Kawaguchi et al./FEMS
Microbiology Letters 126 (1995) 277-282
helix at positions 45-479, which is absent in the
cy-Proteobacteria, is 18 bp long in RS-1, but is 25-27
bp long in other GProteobacteria (e.g. Desuljovibrio
desulfiricans
and Geobacter metallireducens).
At
the signature positions, all nucleotides were those
expected for the &Proteobacteria [26]. The sequence
between positions 687 and 702 was identical to a
sequence specific to the Desulfovibrio subgroup of
the SProteobacteria [27].
3.2. Phylogenetic
analysis
The 16s rDNA sequences in the GenBank and
EMBL. databases with which the 16s rDNA of RS-1
was most similar were those from Geobacter metallireducens and Desulfovibrio spp. (Table 1). RS-1
represents a distinct phylogenetic lineage within the
SProteobacteria (Fig. 2). Several physiological properties of RS-1 are characteristic of sulfate-reducing
members of the SProteobacteria [28], and are therefore consistent with placement in the SProteobacteria. For example, RS-1 precipitates extracellular
iron sulfide by dissimilatory sulfate reduction, and
uses pyruvate, malate, lactate, fumarate and ethanol
as electron donors in sulfate reduction [20].
3.3. Nucleotide sequence accession numbers
The RS-1 nucleotide sequence data will appear in
the GSDB, DDBJ, EMBL and NCBI databases with
the accession number D43944.
4. Discussion
In this work it was demonstrated that RS-1 is in
the Desulfovibrio sub-group of the SProteobacteria
[27]. RS-1 contains magnetite inclusions, showing
that intracellular magnetite biomineralization is not
restricted to magnetic cY-Proteobacteria. However,
rectangular magnetic inclusions may be restricted to
magnetic a-Proteobacteria, as RS-1 magnetic inclusions are bean-shaped [20], and those of other magnetic SProteobacteria are irregularly spheroidal
[l&16]. Numerous bacteria contain bullet-shaped
magnetic inclusions, which are of unknown chemistry [29], and Magnetobacterium
bavaricum, the
281
only type to have been phylogenetically analysed, is
not a member of the Proteobacteria [12].
The bacteria to which RS-1 is most closely related
are Desulfovibrio
spp. and Geobacter metallireducens, both of which reduce ferric iron. D. desulfiricans produces siderite (FeCO,) [30], and G. metallireducens produces magnetite [31]. G. metallireducens is non-magnetic, as it releases the magnetite
outside the cell. The phylogenetic relationship between RS-1 and these bacteria raises the issue of the
biological function of bacterial magnetic inclusions.
When magnetic bacteria were discovered it was suggested that the magnetic inclusions have a navigational function [51, and this hypothesis has been
widely accepted [6,7], although no experimental evidence has been published. However, the evolutionary
relationship between RS-1 and non-magnetic bacteria which reduce ferric iron, and in one case synthesize magnetite, raises the possibility that RS-1 reduces ferric iron for metabolic reasons. If this is the
case, the magnetic inclusions in RS-1 may be byproducts of metabolic iron reduction, with no navigational function.
It was previously shown that synthesis of magnetic inclusions is of multiple evolutionary origin
[17]. However, it remained possible that intracellular
magnetite biomineralization had a single evolutionary origin, as all bacteria containing magnetite inclusions were in the cr-Proteobacteria, and therefore
shared a common ancestor with only a relatively
small range of non-magnetic bacteria. However, RS-1
is a member of the GProteobacteria. This suggests
that either intracellular magnetite biomineralization
had several evolutionary origins, or that it had a
single origin followed by lateral transfer of genetic
information between phylogenetic groups. The latter
possibility seems less likely, as magnetite magnetosomes in RS-1 are morphologically different from
those in other bacteria. However, the possibility of
lateral transfer between bacterial taxa suggests the
possibility that intracellular magnetite biomineralization in animals [32,33-J and plants [34] may have
originated by lateral genetic transfer from bacteria.
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