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Applied and Environmental Microbiology, April 2000, p. 1715-1719, Vol. 66, No. 4
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Prokaryotic Diversity in Zostera
noltii-Colonized Marine Sediments
Ana
Cifuentes,1
Josefa
Antón,2,*
Susana
Benlloch,1
Andrew
Donnelly,3
Rodney A.
Herbert,3 and
Francisco
Rodríguez-Valera1
División de Microbiología, Universidad Miguel
Hernández, Campus de San Juan, 03550 San Juan,
Alicante,1 and División de
Microbiología, Departamento de Fisiología,
Genética y Microbiología, Universidad de Alicante, 03080 Alicante,2 Spain, and Department of
Biological Sciences, University of Dundee, Dundee DD1 4HN, United
Kingdom3
Received 29 October 1999/Accepted 25 January 2000
 |
ABSTRACT |
The diversity of microorganisms present in a sediment colonized by
the phanerogam Zostera noltii has been analyzed. Microbial DNA was extracted and used for constructing two 16S rDNA clone libraries for Bacteria and Archaea. Bacterial
diversity was very high in these samples, since 57 different sequences
were found among the 60 clones analyzed. Eight major lineages of the
Domain Bacteria were represented in the library. The most
frequently retrieved bacterial group (36% of the clones) was
-Proteobacteria related to sulfate-reducing bacteria.
The second most abundant group (27%) was
-Proteobacteria, including five clones closely related
to S-oxidizing endosymbionts. The archaeal clone library included
members of Crenarchaeota and Euryarchaeota,
with nine different sequences among the 15 analyzed clones, indicating
less diversity when compared to the Bacteria organisms.
None of these sequences was closely related to cultured
Archaea organisms.
| |
TEXT |
Our objective in this study was to
describe the diversity of the prokaryotic community inhabiting a marine
sediment colonized by the marine phanerogam Zostera noltii
located in the Bassin d'Arcachon, South-West France. This is a
macrotidal coastal lagoon that represents the most extensive intertidal
meadows of this rooted phanerogam in Western Europe (70 km2). This seagrass ecosystem is characterized by a high
iron content, 111.5 (dry weight) µg/g (32) in the
sediment, as well as strong tidal activity, which ensures regular
mixing of the water body and exposes the sediment surface to the air
for between 4 and 8 h each day. This environment is different from
those that have previously been studied by molecular methods due to the
presence of Z. noltii roots and rhizomes. A number of recent
studies have shown that living seagrasses release dissolved organic
carbon, which can significantly influence the composition and activity of the seagrass rhizosphere microflora (24, 36). For
example, several studies have demonstrated high rates of heterotrophic nitrogen fixation in the rhizosphere of Z. noltii-colonized
sediments which are coupled to the photosynthetic activity of the
plants via the release of fixed carbon from the roots (20, 24,
36). Similarly, substantial stimulation of sulfate reduction
rates in seagrass-colonized sediments in the light have been reported (4, 25). These data indicate a close interaction between the
plants and the microbial community in the rhizosphere.
Samples.
Z. noltii-colonized sediment cores (5-cm
diameter) were collected from Station A in the Bassin d'Arcachon in
July 1996 and kept in the dark at 
20°C until processed. Station A
is located in the center of the Bay, in an open zone subjected to
marine influences. Sediment cores that contained extensive rhizome
material were sliced into sections (1-cm thick, from the surface), and horizon 2 (1 to 2 cm) was chosen for the microbial community analysis.
DNA extraction and purification.
A combination of the methods
described by Zhou et al. (37) and Gray and Herwig
(14) was used. Eight hundred milligrams of sediments were
mixed with 2.16 ml of lysis buffer (100 mM Tris-HCl [pH 8.0], 100 mM
Na EDTA [pH 8.0], 100 mM NaP [pH 8.0], 1.5 M NaCl, and 1%
[wt/vol] cetyltrimethylammonium bromide) and 16 µl of proteinase K
(14 mg/ml). Two-milliliter vials containing 2 g of 0.1-mm zirconia
beads were filled with this mixture and shaken horizontally at 225 rpm
for 30 min at 37°C. After shaking, 480 µl of 10% (wt/vol) sodium
dodecyl sulfate were added. The content of the tubes were homogenized
for 1 min on a Mini Bead Beater Cell Disrupter (Biospec Products,
Bartlesville, Okla.) at maximum setting and then incubated in a 65°C
water bath for 2 h with gentle end-over-end inversions every 10 to
15 min. Samples were centrifuged at 6,000 × g for 10 min, and the supernatants were collected. An equal volume of
chloroform-isoamylalcohol (24:1) was added and then centrifuged at
16,000 × g for 5 min before 0.6 volumes of isopropanol
were added to each tube, incubated at room temperature for 1 h,
and centrifuged at 16,000 × g for 20 min. The
supernatants were decanted, and the pellets were washed with 1 ml of
70% (vol/vol) ice-cold EtOH. The pellets were air dried and
resuspended in 200 µl of sterile deionized water. One hundred
microliters of crude DNA extract was purified with GENECLEAN Spin Kit
(Bio 101, Inc., Vista, Calif.), resuspended into 40 µl of elution
buffer, and electrophoresed on a 1% (wt/vol) agarose gel (Low EEO
agarose; Pronadisa) in 1× Tris-acetate-EDTA at 4 V/cm. The gel was
stained with 0.5 g of ethidium bromide and visualized with UV. The
band larger than 23 kb was excised and purified twice with GENECLEAN columns. Finally, DNA was eluted into 40 µl of elution buffer.
PCR amplification and cloning of PCR products.
Universal
primers for PCR amplification of bacterial and archaeal 16S rRNA genes
were used in this study (forward primer 27f for Bacteria
[16], forward primer 21F for Archaea
[7], and universal reverse primer 1492r
[16] for both Bacteria and
Archaea). PCR was carried out as described previously
(1). Two 16S rDNA clone libraries were constructed, one for
16S rDNA amplified with primers specific for Bacteria
organisms (clone library B2M) and one for Archaea organisms
(clone library A2M). The PCR products obtained from different PCRs were
cloned by using the original TA Cloning Kit (Invitrogen) and following
the manufacturer's recommendations. Inserts were PCR reamplified with
specific primers for the vector and purified with the QIA-quick PCR
Purification Kit (QIAgen) according to the manufacturer's protocol.
The DNA was recovered in 30 µl of water and diluted to a
concentration between 0.3 and 0.5 µg/µl.
Sequencing of 16S rDNAs and data analysis.
Nucleotide
sequences of PCR products were determined by using the ABI PRISM Dye
Terminator Cycle Sequencing Ready Reaction Kit (Perkin-Elmer) according
to the manufacturer's indications. Sixty clones were selected from
B2M, and 15 clones were selected from A2M. For these clones, the 3' end
was partially sequenced with primers Bact1055 and Arc915 (3)
as the sequencing primers for Bacteria and
Archaea, respectively. The 16S rRNA genes of six clones
(B2M-54, B2M-23, B2M-58, B2M-60, B2M-61, and B2M-68) were totally
sequenced by using primers 27f (16), Bact335 (3), Bact785 (3), and 1492r (16). The phylogenetic
affiliation of the obtained sequences was carried out by BLAST at the
National Center for Biotechnology Information (NCBI) web site
(www.ncbi.nlm.nhi.gov) (2). Similarity percentages were
calculated after manual alignment of the clone sequences with that of
the closest relative provided by NCBI. Sequences were submitted to the
CHECK_CHIMERA program at the Ribosomal Database Project (RDP)
(18). For tree calculations, sequences were aligned by using
the Clustal W program (Genetics Computer Group [GCG] Package), and
their similarity matrix was calculated by the Jukes-Cantor method with
the MEGA (Molecular Evolutionary Genetic Analysis) 1.01 program
obtained from the Institute of Molecular Evolutionary Genetics, the
Pennsylvania State University, University Park.
Bacterial 16S rDNA clone library.
Out of the 60 bacterial
clones analyzed, five were of chloroplast origin, which is not
surprising considering that the analyzed sediment was densely colonized
by Z. noltii roots, which have attached diatoms
(11). The remaining 55 (Table
1) were of bacterial origin and fell into
eight major lineages of the Domain Bacteria: 
-, 
-,
-, 
-, and -Proteobacteria, Cytophaga,
Spirochaeta, and gram-positive organisms with a high G+C
content. Among these 55 bacterial sequences analyzed, there were 52 unique sequences, indicating that, firstly, the bacterial diversity in
these sediments was very high and, secondly, that we are far from
establishing the total bacterial diversity of the analyzed samples.
None of the clones was identical to any known 16S rRNA sequence from
cultured organisms or environmental clones.
The most abundant group (24 clones, 44% of the total) was
-
Proteobacteria, and organisms of this group comprised
sequences
(20 clones, 36% of the total) related to sulfur- and
sulfate-reducing
bacteria (SRB). This was also the predominant group in
the 16S
rDNA clone libraries constructed by Gray and Herwig
(
14) and
Ravenslach et al. (
27) when analyzing
marine sediments from
creosote-contaminated Eagle Harbor (Puget Sound,
Washington) and
permanently cold sediments collected off the coast of
Spitsbergen
(Arctic Ocean), respectively. The predominance of SRB in
marine
sediments has been previously demonstrated by direct
quantification
using rRNA slot blot and fluorescent in situ
hybridization (FISH)
analysis (
17,
31). The importance of
SRB in the oxidation
of organic carbon in marine sediments is well
established, since
sulfate is one of the main electron acceptors
present in these
environments. In addition, SRB are able to utilize
different electron
donors available in marine sediments, such as carbon
compounds
released by plant roots (in this case,
Z. noltii)
or fermentation
products of other bacteria, such as acetate, lactate,
butanol,
and formate (
33). Furthermore, several studies
(
6,
19,
21) have shown that some SRB are oxygen tolerant,
which enables
them to colonize microaerophilic habitats, such as plant
roots.
Molecular approaches have been used previously to describe the
diversity of SRB in marine environments since sulfate reduction
is a
major route of organic matter mineralization in these environments
(
15,
34). A number of studies have indicated that marine
sediments
are inhabited by a great diversity of SRB, and new sequences
and
groups are presently being described (
8,
9,
28).
From the same sediment analyzed in this work several SRB have been
isolated:
Desulfospira joergensenii (
12),
Desulfocapsa sulfoexigens (
13), as well as SRB
related to the genera
Desulfovibrio,
Desulfobacter,
Desulfobacula, and
Desulfobacterium (A. Cifuentes,
J. Antón, R. de Wit,
and F. Rodriguez-Valera, unpublished observation).
On the other hand,
Desulfovibrio zosterae (
23) was isolated
from
surface-sterilized roots of the benthic macrophyte
Zostera marina. Interestingly, none of the SRB 16S rDNA sequences directly
retrieved from the environment match those of the isolates mentioned
above. Indeed, we have not recovered sequences related to the
family
Desulfovibrionaceae. These results contrast with those
of
Sahm et al. (
30), who recovered as the most abundant 16S
rDNA sequences the ones that corresponded to SRB frequently isolated
from the same environment (an Arctic marine sediment) affiliated
with
the
Desulfotalea cluster.
The second most abundant group (around 27% of the clones analyzed) in
our clone library was formed by sequences related to
-
Proteobacteria organisms. This group included sequences
related
to bacteria that are readily isolated from marine environments,
like
Pseudomonas spp.,
Aeromonas spp., and
Photobacterium spp.
Remarkably, six of the
-
Proteobacteria-related sequences (clones
B2M-23, B2M-28,
B2M-54, B2M-60, B2M-61, and B2M-68) were related
to sulfur-oxidizing
bacterial endosymbionts. These clones were
fully sequenced, and their
phylogenetic relationship was established
as shown in Fig.
1. Clone B2M-68, which presented a 77.8%
similarity
to the partial sequence (positions 1081 to 1399) of an
Escarpia spicata endosymbiont, was found to be related
(81.8% similarity)
to the
-proteobacterium
Rhizobium
fredii when the complete 16S
rDNA was analyzed. When sequencing
the complete gene, we found
that these sequences were only distantly
related to the endosymbionts
(similarities from 90.8 to 91.9%) but
still clearly associated
with them, as shown in Fig.
1. These sequences
have been also
found in other marine sediments (
27), but
whether they correspond
to free-living bacteria remains unknown.
However, they account
for an important part of the bacterial diversity
recovered in
this study. It is not unreasonable to speculate that these
bacteria,
due to their phylogenetic relationships, are indeed sulfur
oxidizers
that are known to be associated with SRB and may play an
important
role in the detoxification of sulfide, which is toxic to most
living organisms.
View larger version (36K):
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FIG. 1.
Phylogenetic tree from complete 16S rDNA gene of clones
related to sulfur-oxidizing bacterial endosymbionts and reference
strains. The tree was built with the neighbor-joining method by using
the Jukes-Cantor distance estimation. Bootstrap values higher than 50%
are indicated at the main nodes. Nucleotide sequence accession numbers
are as follows: A. phillipiana gill symbiont, L25711;
A. tumefaciens, AH007805; B. pertussis, AF142327;
B. thermophilus gill symbiont, M99445; C. costata
gill symbiont, L25712; C. magnifica symbiont, L25718;
C. orbicularis gill symbiont, X84979; E. coli,
U00096; E. shaposhnikovii, M59151; E. spicata
endosymbiont, U77482; L. mucor, X87277; L. nassula gill symbiont, X95229; N. gonorrhoeae,
AJ239304; N. mobilis, g530889; O. loisae
endosymbiont, AF104475; R. leguminosarum, U89831; R. pachyptila symbiont, U77478; S. occidentalis gill
symbiont, U41049; S. terraeregina gill symbiont, U62131;
S. velum gill symbiont, M90415; T. crunogena,
AF064545; T. flexuosa gill symbiont, L01575; T. gelatinosa, Y11317; T. ramosa, g987512; T. thyasirae, AF016046; V. harveyi, X56578; and Y. leukodermatus endosymbiont, U24110.
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|
The rest of the groups were less abundant:
Cytophaga (three
clones),
-
Proteobacteria (five clones),
Spirochaeta (two clones),
-
Proteobacteria (one clone), and gram-positive and
high G+C content
bacteria (one
clone).
We found two repeated sequences (clones B2M-5, B2M-7, and B2M-13,
93.6% similarity with
Arcobacter skirrowi; clones B2M-19
and B2M-38, 92.7% similarity to
Spirochaeta africana).
Llobet-Brossa
et al. (
17), when analyzing by FISH the
microbial composition
of Wadden Sea sediments, reported a considerable
proportion (1.3%)
of bacteria detectable with a FISH probe
specifically designed
for
Arcobacter spp. This bacterium had
not previously been reported
to be significant in marine sediments.
Arcobacter was only detected
in the upper layer of the
sediments which, according to these
authors, was not surprising,
considering their ability to respire
nitrate. Marine sediments are
typical habitats of spirochetes
(
5). However, sequences
related to
Spirochaeta spp. have not
been found previously
in sediment 16S rDNA libraries (
14,
27)
but, on the other
hand, Rosselló-Mora et al. (
29) found sequences
affiliated to the spirochete phylum when analyzing by denaturing
gradient gel electrophoresis anoxic sediments from the Black
Sea.
Archaeal 16S rDNA clone library.
Fifteen archaeal clones were
partially sequenced, five (clones A2M-27 [identical to clone A2M-28],
A2M-11 [identical to clone A2M-17], and A2M-32) of which were
phylogenetically associated with Crenarchaeota sequences and
ten (clones A2M-2 [identical to clones A2M-3 and A2M-4], A2M-8,
A2M-12, A2M-21, A2M-30, A2M-36, A2M-45, and A2M-57) of which were
phylogenetically associated with Euryarchaeota (see Fig.
2).
View larger version (32K):
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FIG. 2.
Relationships between partial 16S archaeal rDNA gene
clones and reference strains. The tree was constructed as that in Fig.
1. T. thermophilus was used as the outgroup. Nucleotide
sequence accession numbers are as follows: A. brierleyi,
X90477; C. noboribetus, D85038; C. symbiosum,
U51469; crenarchaeotal sp. clone pJP 89, L25305; D. mobilis,
M36474; F. metallovorans, AJ224936; H. salinarium, AJ002947; H. butylicus, X99553; I. islandicus, X99562; M. palustre, AF093061; M. liminatans, Y16428; P. abyssi, X99559; P. fumarius, X99555; S. acidocaldarius, D14053; T. waimanguensis, AF098975; T. thermophilus, X07998;
uncultured archaeon WCHD3-16, AF050618; and uncultured archaeon
WCHD3-02, AF050616.
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|
Three of the
Crenarchaeota-related clones (A2M-11 and
A2M-17, which are identical, and A2M-32) were distantly related to
Cenarchaeum symbiosum, a marine archaeon that inhabits the
tissues of a temperate
water sponge (
26). Two of the
remaining
Crenarchaeota-related
clones (A2M-27 and A2M-28,
which are identical) were associated
to an environmental clone
retrieved from a hot spring in Yellowstone
National
Park.
Euryarchaeota-related clones were associated with
environmental clones retrieved from an aquifer contaminated with
hydrocarbons
and chlorinated solvents undergoing intrinsic
bioremediation (
10).
Our clones were related to sequences
WCHD3-02 and WCHD3-16 retrieved
from the methanogenic redox sampling
zone.
The presence of
Euryarchaeota in sediments has been widely
reported since methanogens are known to inhabit this kind of
environment.
Although the molecular approaches to the study of archaeal
diversity
in marine sediments are very limited, some authors have also
retrieved
methanogen-related 16S rDNA sequences from these
environments.
Munson et al. (
22) recovered a wide range of
Euryarchaeota sequences
when studying a salt marsh sediment
sample that showed active
methanogenesis and sulfate reduction. These
authors were unable
to find any sequence related to those of
Crenarchaeota organisms.
However, in this study, several
Crenarchaeota-related clones were
identified. The presence
of
Crenarchaeota-related sequences in
marine sediments has
been described previously (
35).
Since we are working with partial sequences that present very low
similarity with cultured
Archaea organisms, it is not
possible
from these limited data to comment on their ecological role in
these sediments. However, it is evident that
Archaea
organisms
other than methanogens may be an important part of the
prokaryotic
community in marine
sediments.
Nucleotide sequence accession numbers.
The sequences from this
study are available through GenBank under accession no. AF218422 to
AF218430 and AF223253 to AF223307.
| |
ACKNOWLEDGMENTS |
This work was supported by European Commission Grant ENV4-CT96-0218
and Spanish Government CICYT AMB96-2484-CE. European Land-Ocean Interaction Studies (ELOISE) contribution number 128. A.C. was a
Generalitat Valenciana fellowship holder.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: División
de Microbiología, Departamento de Fisiología,
Genética y Microbiología, Universidad de Alicante, Apto.
99, San Vicente del Raspeig, 03080 Alicante, Spain. Phone: 965903870. Fax: 965909494. E-mail: anton{at}ua.es.
| |
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Applied and Environmental Microbiology, April 2000, p. 1715-1719, Vol. 66, No. 4
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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