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Applied and Environmental Microbiology, July 2000, p. 2797-2803, Vol. 66, No. 7
Shimizu Laboratories, Marine Biotechnology
Institute, Shimizu City, Shizuoka 424-0037, Japan
Received 24 January 2000/Accepted 24 April 2000
The growth of marine bacteria under iron-limited conditions was
investigated. Neither siderophore production nor bacterial growth was
detected for Pelagiobacter sp. strain V0110 when Fe(III) was present in the culture medium at a concentration of <1.0 µM. However, the growth of V0110 was strongly stimulated by the presence of
trace amounts of exogenous siderophore from an alpha proteobacterium, V0902, and 1 nM N-acyl-octanoylhomoserine lactone
(C8-HSL), which is known as a quorum-sensing chemical
signal. Even though the iron-binding functionality of a hydroxamate
siderophore was undetected in the supernatant of V0902, a hydroxamate
siderophore was detected in the supernatant of V0110 under the above
conditions. These results indicated that hydroxamate siderophore
biosynthesis by V0110 began in response to the exogenous siderophore
from V0902 when in the presence of C8-HSL; however,
C8-HSL production by V0110 and V0902 was not detected.
Direct interaction between V0902 and V0110 through siderophore from
V0902 was observed in the dialyzing culture. Similar stimulated growth
by exogenous siderophore and HSL was also observed in other
non-siderophore-producing bacteria isolated from marine sponges and
seawater. The requirement of an exogenous siderophore and an HSL for
heterologous siderophore production indicated the possibility that
cell-cell communication between different species was occurring.
Iron is an essential element for all
microorganisms (37, 43). To survive under iron-deficient
conditions, terrestrial microorganisms produce siderophores,
low-molecular-mass iron-chelating compounds which bind iron with high
affinity (Kaff > 1030)
(26). Due to the low iron concentration (<0.4 µM) in the
ocean, marine bacteria are thought to be capable of producing
siderophores (14, 41); however, few marine siderophores have
been identified (22, 32). Recent geochemical investigations
on the distribution of iron in seawater have demonstrated that more
than 99.9% of the dissolved iron in the surface ocean is bound to
organic compounds (13, 18, 33, 44). The chemical nature of
these organic compounds is uncertain. Due to high binding activities
with Fe(III), siderophores biosynthesized by marine bacteria are a
likely candidate for the iron-binding organic compounds in the ocean.
It has been reported that siderophore biosynthesis in the pathogenic
bacterium Pseudomonas aeruginosa is controlled by a
quorum-sensing system (39). Quorum sensing is
cell-density-dependent regulation of specific gene expression in
response to extracellular chemical signals produced by the bacteria
themselves (9). In a wide range of gram-negative bacteria,
quorum sensing was identified to be based on one or more
N-acyl homoserine lactones (HSLs) (11). All HSLs
thus far reported are composed of an acyl chain with an even number of
carbon atoms ranging from 4 to 14 in length, ligated to the homoserine
lactone moiety (38). Although quorum-sensing-related siderophore biosynthesis has also been reported in the pathogenic bacterium Burkholderia cepacia (20), siderophores
produced by this strain and P. aeruginosa were thought to be
the virulence factors related to their pathogenesis. No
quorum-sensing-controlled siderophore biosynthesis system has been
found from the open ocean.
Recent investigations have reported that iron availability limits
phytoplankton growth in large areas of the world's oceans and may
influence biological carbon flow (4, 5, 21). The response of
bacteria to iron enrichment has also been investigated, and marine
bacteria were found to contain more iron per biomass than phytoplankton
(40, 41). Iron uptake competition among phytoplankton
through different siderophores has also been reported (16).
It is suggested that siderophores produced by marine bacteria may be a
very important factor which affects the "iron flow" in the ocean
among bacteria or between bacteria and other microorganisms. To
understand such bacterial communication related to iron uptake activity
through siderophores in the ocean, we focused on the influence of
siderophores and on quorum-sensing chemical signals during bacterial
growth under iron-limited poor nutrient conditions similar to those of
the natural ocean. In the present study, stimulated bacterial growth in
the presence of siderophores and synthetic HSLs under iron-deficient
conditions was reported.
Strains and culture conditions.
Bacteria were isolated from
17 different marine sponges collected in Fiji and from seawater from
four locations near Japan. The sponge tissue was squeezed, the
solutions obtained were diluted from 10
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Bacterial Growth Stimulation with Exogenous
Siderophore and Synthetic N-Acyl Homoserine Lactone
Autoinducers under Iron-Limited and Low-Nutrient Conditions
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
1 to
104 times in sterilized seawater, and 100 µl of each
solution was spread onto 1/10-diluted marine broth (Marine Broth 2216;
Difco) agar plates. The plates were incubated at 30°C, and marine
bacteria were identified by growth on the plates containing 3% NaCl in comparison with no growth on the agar plates containing 0.15% NaCl for
the same strain.
Pelagiomicin production. Pelagiomicin production by strain V0110 was determined by the following methods. After culturing of strain V0110 in marine broth liquid medium at 30°C for 24 h, the supernatant was collected by centrifugation and was extracted with CHCl3. The organic extract was concentrated to dryness. The residue was dissolved in 10 mM phosphate buffer (pH 7.0) and was analyzed by high-pressure liquid chromatography (HPLC) (Shiseido Capcell-CN column; 15 by 25 mm) at 265 nm. The elution gradient consisted of CH3CN in phosphate buffer (pH 7.0). HPLC active fraction was confirmed to be pelagiomicin A by analysis of nuclear magnetic resonance (NMR) spectra (17).
Siderophore detection.
The chrome azurol S (CAS) assay
(35) was used to detect siderophores. On CAS agar plates,
siderophore-producing (Sid+) bacteria form colonies with an
orange halo. This occurs because iron is removed from the original blue
CAS-Fe(III) complex during siderophore production. Formation of
siderophore halos was evaluated following 5 days of colony incubation
at 30°C. The CAS solution assay (14, 35) was used to
quantitate siderophore activity in culture supernatant extract by
measuring the decrease in the absorbance of blue color at 630 nm.
Standard curves relating CAS reactivity to the iron-binding ligands
were determined using the fungal siderophore desferrioxamine (Desferal;
CIBA-GEIGY). The quantity of siderophores produced by the bacteria was
reported in terms of iron-binding equivalents, expressed as moles per
gram (dry weight) of bacteria (14). Hydroxamate and catechol
functionality of 10-fold-concentrated siderophore extracts of V0902 and
V0110 were examined by the Csaky test (12) and the Arnow
reaction (1), respectively. In these assays, hydroxylamine
and 2,3-dihydroxybenzoic acid, respectively, were used as the
standards. Strains which neither grew nor formed a halo on the CAS agar
plates containing different Fe(III) concentrations (104
to 10 µM) were defined as non-siderophore-producing
(Sid) bacteria.
Isolation of siderophores. Bacterial cultures grown in 200 ml of IDSM medium for 2 days at 30°C were harvested by centrifugation at 8,000 rpm for 30 min. Iron-free siderophores were obtained by the following method. The supernatant was filtered through a 0.2-µm (pore-size) membrane filter to completely remove the cells and was acidified to pH 3 with concentrated HCl. Supernatants were extracted three times with equal volumes of ethyl acetate for catechols and benzyl alcohol for hydroxamates (27). The concentrated organic extracts were dissolved in 1 ml of a buffer (0.01 M phosphate buffer [pH 7.0] or 0.01 M acetate buffer [pH 4.0]). Partial purification of the siderophores was achieved by the fractionation of the organic extracts on a Sephadex LH-20 (Pharmacia) column in the respective buffers. The eluting solutions were purified with Chelex-100 to remove the iron. The CAS assay-reactive fractions were pooled and concentrated 10-fold by lyophilization.
Chemical synthesis of HSLs. N-(3-Oxohexanoyl)-L-HSL was prepared according to the procedure of Chhabra et al. (3). N-(3-Oxooctanoyl)-, N-(3-oxodecanoyl)-, and N-(3-oxododecanoyl)-L-HSLs were synthesized as described previously (34, 46). The final products were purified by silica gel column chromatography (Merck Kieselgel 60, CHCl3-MeOH) followed by ODS open column chromatography (Cosmosil 5C18-AR; MeOH-H2O). Synthesis of N-[(S)-3-hydroxybutyryl]-L-HSL was as previously described (2). Unsubstituted acyl HSLs were synthesized as follows. Triethylamine (1.1 eq) and pyridine (1.5 eq) were successively added to a suspension of L-HSL hydrochloride (2.5 mmol) in anhydrous CH2Cl2 (10 ml) at 0°C. To this mixture, the corresponding acyl chloride (1.1 eq) was added dropwise. The mixture was stirred at room temperature overnight and poured into 1 M HCl. The aqueous layer was extracted with CH2Cl2, and the combined organic layer was dried over Na2SO4, filtrated, and concentrated to give an unsubstituted acyl HSL as a colorless powder. The purity of the synthetic HSL was checked by thin-layer chromatography (TLC), HPLC, and NMR.
Agrobacterium tumefaciens A136 reporter strain
assay.
The A. tumefaciens A136/(pCF218)(pCF372)
reporter strain was kindly supplied by Clay Fuqua (University of
Indiana) (10). This strain has been reported to detect a
wide range of HSL compounds, including compounds with acyl chains of
greater than four carbons and compounds with 3-oxo- or 3-hydroxyl
substituents, including compounds that were unsubstituted at this
position. After cultivation of the strain in 100 ml of IDSM medium or
Marine Broth 2216 to stationary phase, the supernatant was collected by
centrifugation at 8,000 rpm for 10 min. The supernatant was extracted
with an equal volume of ethyl acetate three times. The combined organic fraction was dried over Na2SO4, concentrated,
and dissolved in 100 µl of methanol and applied to a reversed-phase
TLC system (Merck HPTLC plate RP-18 WF254S, 10 by 9 cm;
60% MeOH in water). HSL autoinducers were detected by TLC overlay
assay using the reporter strain immobilized in the agar that contained
the chromogenic X-Gal
(5-bromo-4-chloro-3-indolyl-
-D-galactopyranoside)
(36, 47). HSL autoinducers cause the formation of blue spots
on the TLC plates. The synthetic HSLs were used as standards.
3,
103, 104, and 1 nM, respectively.
Cross-feeding assay for Sid bacteria with exogenous
siderophores and synthetic HSLs.
Sid strains were
inoculated on four different CAS plates: (i) without any addition, (ii)
with the addition of an exogenous siderophore, (iii) with the addition
of an HSL, and (iv) with the addition of an exogenous siderophore plus
an HSL. The exogenous siderophore was added to the plates by spreading
500 µl of filtered siderophore extract (0.155 nmol of ligands/g [dry
weight]) buffer-dissolved solution from Sid+ strain V0902.
Each HSL was added by spreading 100 µl of different concentrations
(103 to 101 µM) of synthetic HSL solution.
Plates and colonies were observed after incubation at 30°C for 7 days.
Dialyzing cultures of Sid strain V0110 and
Sid+ strain V0902.
A dialyzing culture of V0902 and
V0110 was designed in Centriprep centrifugal filters (Amicon). The
Centriprep centrifugal filter consists of two parts: a sample container
and a filtrate collector with a low adsorptive regenerated cellulose
dialyzing membrane. Centriprep-10 (nominal molecular weight limit,
10,000) was used because it has a wide range for compounds to pass
through the membrane easily. The integrity of the Centriprep membrane after heat sterilization was checked by cultivating the bacteria in the
filtrate collector or the sample container at 30°C for 14 days and
spreading the cultures onto marine broth agar plates. No bacteria were
found to pass through the membrane. The Sid+ strain V0902
was inoculated into the sample container with 5 ml of IDSM medium. The
Sid strain V0110 was inoculated into the filtrate
collector with 5 ml of IDSM medium plus 1 nM synthetic
C8-HSL. The filtrate collector was positioned with the
air-seal cap to give a 0.7-cm space between the membrane support base
and the bottom of the sample container. The Centriprep-10 was shaken at
100 rpm at room temperature for 7 days. Then, 100 µl of each culture
was collected every 24 h, and the OD600 was measured
using a Beckman spectrophotometer DU640 to estimate the bacterial growth.
Nucleotide sequence accession number. The DDBJ GenBank accession number of the sequence for V0902 is AB012864.
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RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Siderophore and HSL production of marine bacterial strains V0110 and V0902. The marine bacterial strains V0110 and V0902 were isolated from the marine sponges Jaspis joinstoni and Plakortis lita de Laubenfels, respectively. They were identified as marine species by their halophilic growth (NaCl > 3.0%). The 16S rDNA sequence of V0110 is 98% identical to that of the marine bacterium Pelagiobacter variabilis, which is a halophilic gram-negative bacterium isolated from a macroalga (17). Pelagiomicin antibiotic production has only been reported in this genus (17). Production of pelagiomicin A (3.6 mg/liter) by strain V0110 also indicated that this bacterium is a Pelagiobacter sp. The 16S rDNA sequence of V0902 is 97% identical to that of an alpha proteobacterium (AB012864 [DDBJ]).
The bacterial growth of V0110 and V0902 under iron-deficient conditions was investigated with 0.1 µM Fe(III)-containing marine broth agar plates. V0902 was observed to form colonies for generations on the iron-deficient agar plate, while no colonies were observed for V0110. Siderophore production by V0902 and V0110 was investigated using the CAS agar plates. Strain V0110 was shown to be a Sid
strain by screening on CAS agar plates which contained
104 to 10 µM Fe(III). Strain V0902 showed siderophore
production on CAS agar plates and was categorized to be a
Sid+ strain. The siderophore component from V0902 was
partially purified by extraction with ethyl acetate or benzyl alcohol
(27) and was evaluated by the CAS solution assay (14,
35). The CAS assay result indicated that strain V0902 produced
ca. 0.31 µmol of iron ligands per g (cell dry weight) after
cultivation in 200 ml of IDSM medium (Table
1).
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|
Stimulated growth of V0110 with the addition of exogenous
siderophore and C8-HSL.
A cross-feeding assay for
V0110 was performed on CAS agar plates with the addition of each
siderophore extract (0.155 nmol/g [dry weight]) from V0902 or of one
of the HSLs at 1 nM or with the addition of a siderophore extract from
V0902 plus one of the HSLs at 1 nM. V0110 was observed to grow only on
the agar plate that contained both the siderophore extract from V0902
and 1 nM C8-HSL (Fig. 2 and
Table 2). Figure 2 shows the colony
formation of V0110 on the CAS plate with the above-described additions. The siderophore component from V0902 added to the CAS agar plate was
0.155 nmol of iron ligands/g (dry weight), and this amount was 200 times less than that used for the CAS assay. This amount did not induce
any color change on the CAS agar plates. The colony halo indicated the
possible siderophore production by V0110.
|
|
= 600 nm) over 4 days. These results coincided with
observations on the CAS agar plate shown in Fig. 2.
|
Dialyzing culture of V0902 and V0110.
To analyze direct
interactions between the Sid strain V0110 and the
Sid+ strain V0902, simultaneous cultivation of the two
strains in Centriprep centrifugal filters was designed. The monitored
growth of both strains in the dialyzing culture or independent culture is shown in Fig. 4. In the presence of 1 nM C8-HSL, the bacterial growth of the Sid
strain V0110 was not detected during the first 2 days and started after
strain V0902 reached stationary phase. The same stimulated growth of
V0110 in the presence of 1 nM C8-HSL was observed when 0.155 nmol/g (dry weight) of siderophore extract from V0902 was added
to the sample container instead of the inoculation of strain V0902
(data not shown). The growth of V0110 in an independent culture with
the direct addition of siderophore extract was observed to be faster
than that seen in dialyzing culture, but the maximum cell density was
almost the same (data not shown). No growth was observed without
C8-HSL under any conditions of dialyzing cultivation (Fig.
4A). The growth of Sid+ strain V0902 under dialyzing
cultivation with Sid strain V0110 showed a higher density
than that seen under independent cultivation with an equal starting
cell number.
|
, V0902; 
, V0110 with 1 nM
C8-HSL; 
, without C8-HSL. (B) Comparison of
dialyzing culture (
) of V0902 in 5 ml
of IDSM medium in a Centriprep-10 centrifugal filter at room
temperature for 7 days. The data represent the averages of three
measurements.
Influence of exogenous siderophores and autoinducers on
Sid marine bacteria from sponges and seawater.
To
estimate whether the effect of the exogenous siderophore and the HSL
autoinducer is a specific activity of V0110 or is universal for marine
bacteria, we investigated another 20 Sid bacteria which
did not respond by growth to exogenous siderophore from V0902. Table 2
shows the positive results of bacterial colony and siderophore halo
formation with the addition of exogenous siderophore from V0902 and one
of nine HSLs on CAS agar plates. All strains shown were
Sid and non-HSL-producing bacteria as determined by CAS
plate and A. tumefaciens A136 reporter strain assays. The
stimulated growth of such Sid strains under iron-limited
conditions was similar to that observed with strain V0110 when
incubated in the presence of the V0902 siderophore and
C8-HSL. It is interesting that more than one kind of
autoinducer showed a positive result in the same strain such as in
C10, where the bacterial growth of V0110 was stimulated in
response to the same siderophore. However, the HSLs with butanoyl chains did not affect any tested Sid strains here.
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Some terrestrial Sid bacteria have been reported to
survive under iron stress in the presence of exogenous siderophores
(30, 31). However, it is not clear whether those bacteria
might be stimulated to synthesize their own siderophores. Only the
Csaky assay gave a positive result for siderophore extract from V0110 cultured with a trace amount of siderophore extract from V0902 and
C8-HSL, while siderophore extract from V0902 gave a
negative result in both of the assays. This finding indicates that a
hydroxamate siderophore was synthesized by V0110 only in the presence
of trace amounts of exogenous siderophore from V0902 and
C8-HSL autoinducer. This phenomenon has not been reported
before. The dialyzing culture of V0110 and V0902 also indicates direct
bacterial interaction through siderophores in the presence of HSL. The
growth of V0110 in the dialyzing culture with C8-HSL
suggests that the siderophore produced by V0902 in the sample container
diffused to the filtrate collector through the membrane and enabled the
growth of V0110 to commence after 2 days. It is well known that
siderophore production reaches a peak level in the stationary phase
(27). The independent culture of V0110 with the direct
addition of siderophore extract and C8-HSL was more rapid
in the growth than in the dialyzing culture. The 2-day delay in the
commencement of V0110 growth in the dialyzing culture might be due to
the delay in reaching the threshold concentration of V0902 siderophore
in the filtrate collector. Almost the same maximum cell density was
observed for V0110 in both the dialyzing and the independent cultures.
This result indicates that the growth rate of V0110 does not depend on
the amount of siderophore from V0902 and thus suggests that the
siderophore from V0902 is a signal for V0110 to commence synthesis of
its own hydroxamate siderophore. Direct interaction of V0110 and V0902 through the siderophores suggests that siderophores might be a signal
for interspecies bacterial communication.
Quorum-sensing-controlled siderophore production has been shown to occur in P. aeruginosa (39) and B. cepacia (20). Quorum-sensing systems in gram-negative bacteria have been well studied (9), and HSLs have been known to be the membrane-permeable signaling molecule. So far, most of the quorum sensing has been found to occur in symbiotic or pathogenic interactions. It is not unexpected that V0110, which was isolated from a marine sponge, responds to HSL signaling because a marine sponge is a symbiotic organism with large amounts of bacteria and microalgae. The requirement of C8-HSL or C10-HSL for the stimulated biosynthesis of heterologous siderophore indicates that HSL also might be a signaling molecule for V0110. No production of C8-HSL and C10-HSL was detected in V0110 and V0902 by the A. tumefaciens A136 reporter strain assay. This suggests possible interspecies communication through C8-HSL or C10-HSL produced by other species. Communication between different species through HSLs has been reported in Vibrio harveyi for its bioluminescence (15) and during B. cepacia for its production of virulence factors (24). McKenney et al. (24) reported that siderophore production by B. cepacia was observed to increase sevenfold when supernatant from Sid+ P. aeruginosa PAO1 was added to Sid+ B. cepacia. P. aeruginosa PAO1 was known to produce C4 and 3OC12-HSLs (28, 29), while B. cepacia was observed to produce C4-, C6-, and 3OC6-HSLs (24). Siderophore production by B. cepacia with the addition of the supernatant of lasR deletion mutant P. aeruginosa PAO-RI was higher than that with the addition of the supernatant of B. cepacia. The P. aeruginosa PAO-RI mutant has been shown to produce 1,000- and 20-fold-less 3OC12-HSL and C4-HSL, respectively, than the wild-type strain P. aeruginosa PAO1 (29). Those suggested that the increased siderophore production by B. cepacia may be stimulated by other undetected HSLs in the P. aeruginosa PAO-RI mutant (24). Our study suggests that siderophores produced by P. aeruginosa PAO1 were possible corporate signals with HSLs which stimulated the siderophore production by B. cepacia.
Stimulated growth by exogenous siderophores and HSLs was also observed
in marine planktonic Sid bacteria. This suggests that
such interspecies communication may occur in an open aquatic
environment. The interactions through siderophores and HSLs between
marine bacteria may be one of the factors which affects the uptake of
iron by bacteria. These findings contribute useful information to our
knowledge of "iron flow" between different microorganisms in the ocean.
Bacteria are abundant in the ocean; however, <0.1% of these bacteria are thought to have been isolated. The majority are believed to be nonculturable species since most marine bacteria cannot be cultivated by traditional microbiological protocols (45). The marine bacterium, V0110, studied here, for example, is unculturable under iron-limited stress, but this stress can be alleviated with an exogenous siderophore and a quorum-sensing chemical signal such as HSL. Thus, it may be possible to isolate marine species under natural, aqueous, nutrient-poor conditions with the addition of trace siderophores and autoinducers.
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ACKNOWLEDGMENTS |
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This work was performed as a part of The Industrial Science and Technology Project, Technological Development of Biological Resources in Bioconsortia, supported by New Energy and Industrial Technology Development Organization.
We thank Clay Fuqua, University of Indiana, for kindly supplying us with the reporter strain. We also are grateful for the support of Y. Shizuri, Marine Biotechnology Institute, Shimizu Laboratories.
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FOOTNOTES |
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* Corresponding author. Shimizu Laboratories, Marine Biotechnology Institute, 1900 Sodeshi-cho, Shimizu City, Shizuoka 424-0037, Japan. Phone: 81-543-66-9215. Fax: 81-543-66-9256. E-mail: lguan{at}shimizu.mbio.co.jp.
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REFERENCES |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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|---|
| 1. | Arnow, L. E. 1937. Colorimetric determination of the components of 3,4-hydroxyphenylalanine-tyrosine mixtures. Annu. Rev. Biochem. 50:715-731[CrossRef]. |
| 2. |
Cao, J.-G., and E. A. Meighen.
1993.
Biosynthesis and stereochemistry of the autoinducer controlling luminescence in Vibrio harveyi.
J. Bacteriol.
175:3856-3862 |
| 3. | Chhabra, S. R., P. Stead, N. J. Bainton, G. P. C. Salmond, G. S. A. B. Stewart, P. Williams, and B. W. Bycroft. 1993. Autoregulation of carbapenem biosynthesis in Erwinia carotovora by analogues of N-(3-oxohexanoyl)-L-homoserine lactone. J. Antibiot. 46:441-454[Medline]. |
| 4. | Coale, K. H., S. E. Fitzwater, R. M. Gordon, K. S. Johnson, and R. T. Barber. 1996. Control of community growth and export production by upwelled iron in the equatorial Pacific Ocean. Nature 379:621-624[CrossRef]. |
| 5. | de Baar, H. J., W. de Jong, J. T. M. Bakker, B. M. Loscher, C. Veth, U. Bathmann, and V. Smetacek. 1995. Importance of iron for plankton blooms and carbon dioxide drawndown in the Southern Ocean. Nature 373:412-415[CrossRef]. |
| 6. | Dominique, P. A. G., B. Mottle, D. W. Morck, M. R. W. Brown, and J. W. Costerton. 1990. A simplified rapid method for the removal of iron and other cations from complex media. J. Microbiol. Methods 12:13-22. |
| 7. | Eberhard, A., A. L. Burlingame, C. Eberhard, G. L. Kenyon, K. H. Nealson, and N. J. Oppenheimer. 1981. Structural identification of autoinducer of Photobacterium fischeri. Biochemistry 20:2444-2449[CrossRef][Medline]. |
| 8. | Eberhard, A., C. A. Widrig, P. McBath, and J. B. Schineller. 1986. Analogs of the autoinducer of bioluminescence in Vibrio fischeri. Arch. Microbiol. 155:294-297[CrossRef]. |
| 9. | Fuqua, C., S. C. Winans, and E. P. Greenberg. 1996. Census and consensus in bacterial ecosystem: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu. Rev. Microbiol. 50:727-751[CrossRef][Medline]. |
| 10. |
Fuqua, C., and S. C. Winans.
1996.
Conserved cis-acting promoter elements are required for density-dependent transcription of Agrobacterium tumefaciens conjugal transfer genes.
J. Bacteriol.
178:435-440 |
| 11. | Fuqua, C., and A. Eberhard. 1999. Signal generation in autoinduction systems: synthesis of acylated homoserine lactones by LuxI-type proteins, p. 211-230. In G. M. Dunny, and S. C. Winans (ed.), Cell-cell signaling in bacteria. American Society for Microbiology, Washington, D.C. |
| 12. | Gillam, A. H., A. G. Lewis, and R. J. Andersen. 1981. Quantitative determination of hydroxamic acids. Anal. Chem. 53:841-844[CrossRef]. |
| 13. | Gledhill, M., and C. M. G. van der Berg. 1994. Determination of complexation of iron (III) with natural organic complexing ligands in seawater using cathodic stripping voltammetry. Mar. Chem. 47:41-54[CrossRef]. |
| 14. | Granger, J., and N. M. Price. 1999. The importance of siderophores in iron nutrition of heterotrophic marine bacteria. Limnol. Oceanogr. 44:541-555. |
| 15. | Greenberg, E. P., J. W. Hastings, and S. Ulizur. 1979. Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch. Microbiol. 120:87-91[CrossRef]. |
| 16. | Hutchins, D. A., A. E. Witter, A. Bulter, and G. W. Luther, III. 1999. Competition among marine phytoplankton for different chelated iron species. Nature 400:858-861. |
| 17. | Imamura, N., M. Nishijima, T. Taketera, K. Adachi, M. Sakai, and H. Sano. 1997. New anticancer antibiotics pelagiomicins, produced by a new marine bacterium Pelagiobacter variabilis. J. Antibiot. 50:8-12[Medline]. |
| 18. | Johnson, K. S., R. M. Gordon, and K. H. Coale. 1997. What controls dissolved iron concentrations in the world ocean? Mar. Chem. 57:137-161[CrossRef]. |
| 19. |
Kuo, A.,
N. V. Blough, and P. V. Dunlap.
1994.
Multiple N-acyl-L-homoserine lactone autoinducers of luminescence in marine symbiotic bacterium Vibrio fischeri.
J. Bacteriol.
176:7558-7565 |
| 20. |
Lewenza, S.,
B. Conway,
E. P. Greenberg, and P. A. Sokol.
1999.
Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI.
J. Bacteriol.
181:748-756 |
| 21. | Martin, J. H., and S. E. Fitzwater. 1988. Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic. Limnol. Oceanogr. 36:1793-1802. |
| 22. |
Martinez, J. S.,
G. P. Zhang,
P. D. Holt,
H.-T. Jung,
C. J. Carrano,
M. G. Haygood, and A. Bulter.
2000.
Self-assembling amphiphilic siderophores from marine bacteria.
Science
287:1245-1247 |
| 23. |
McClean, K. H.,
M. K. Winson,
L. Fish,
A. Taylor,
S. R. Chhabra,
M. Camara,
M. Daykin,
J. H. Lamb,
S. Swift,
B. W. Bycroft,
G. S. A. B. Stewart, and P. Williams.
1997.
Quorum sensing and Chromobacterium violaceum: exploitation and violacein production and inhibition for the detection of N-acylhomoserine lactone.
Microbiology
143:3703-3711 |
| 24. |
McKenney, D.,
K. E. Brown, and D. G. Allison.
1995.
Influence of Pseudomonas aeruginosa exoproducts on virulence factor production in Burkholderia cepacia: evidence of interspecies communication.
J. Bacteriol.
177:6989-6992 |
| 25. |
Milton, D. L.,
A. Hardman,
M. Camara,
S. R. Chhabra,
B. W. Bycroft,
G. S. A. B. Stewart, and P. Williams.
1997.
Quorum sensing in Vibrio anguillarum: characterization of the vanI/vanR locus and identification of the autoinducer N-(3-oxodecanoyl)-L-homoserine lactone.
J. Bacteriol.
179:3004-3012 |
| 26. |
Neilands, J. B.
1995.
Siderophores: structure and function of microbial iron transport compounds.
J. Biol. Chem.
270:26723-26726 |
| 27. | Payne, S. M. 1994. Detection, isolation, and characterization of siderophores. Methods Enzymol. 235:329-344[Medline]. |
| 28. |
Pearson, J. P.,
K. M. Gray,
L. Passador,
K. D. Tucker,
A. Eberhard,
B. H. Iglewski, and E. P. Greenberg.
1994.
Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence gene.
Proc. Natl. Acad. Sci. USA
91:197-201 |
| 29. |
Pearson, J. P.,
K. L. Passador,
B. H. Iglewski, and E. P. Greenberg.
1995.
A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa.
Proc. Natl. Acad. Sci. USA
92:1490-1494 |
| 30. |
Poole, K.,
L. Young, and S. Nesshat.
1990.
Enterobactin-mediated iron transport in Pseudomonas aeruginosa.
J. Bacteriol.
172:6991-6996 |
| 31. |
Rabsch, W.,
W. Voigt,
R. Reissbrodt,
R. M. Tsolis, and A. J. Baumler.
1999.
Salmonella typhimurium TroN and FepA proteins mediated uptake of enterobactin but differ in their specificity for other siderophores.
J. Bacteriol.
181:3610-3612 |
| 32. | Reid, R. T., D. H. Live, D. J. Falkner, and A. Bulter. 1993. A siderophore from a marine bacterium with an exceptional ferric iron affinity constant. Nature 366:455-458[CrossRef][Medline]. |
| 33. | Rue, E. L., and K. W. Bruland. 1995. Complexation of iron(III) by natural ligands in the Central North Pacific as determined by a new competitive ligand equilibration/adsorptive cathodic stripping voltammetric method. Mar. Chem. 50:117-138. |
| 34. |
Schaefer, A. L.,
B. L. Hanzelka,
A. Eberhard, and E. P. Greenberg.
1996.
Quorum sensing in Vibrio fischeri: probing autoinducer-LuxR interactions with autoinducer analogs.
J. Bacteriol.
178:2897-2901 |
| 35. | Schwyn, B., and J. B. Neilands. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160:47-56[CrossRef][Medline]. |
| 36. |
Shaw, P. D.,
G. Ping,
S. L. Daly,
J. E. Cronan, Jr.,
K. L. Rinehart, and S. K. Farrand.
1994.
Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography.
Proc. Natl. Acad. Sci. USA
94:6036-6041 |
| 37. | Sigel, A., and H. Sigel (ed.). 1998. Metal ions in biological systems, p. 1-29. Marcel Dekker, Inc., New York, N.Y. |
| 38. | Simon, S., P. Williams, and G. S. A. B. Stewart. 1999. N-Acylhomoserine lactones and quorum sensing in proteobacteria, p. 291-313. In G. M. Dunny, and S. C. Winans (ed.), Cell-cell signaling in bacteria. American Society for Microbiology, Washington, D.C. |
| 39. | Stintzi, A., K. Evans, J. M. Meyer, and K. Poole. 1998. Quorum-sensing and siderophore biosynthesis in Pseudomonas aeruginosa: lasR/lasI mutants exhibit reduced pyoverdine biosynthesis. FEMS Microbiol. Lett. 15:341-345[CrossRef]. |
| 40. | Tortell, P. L., M. T. Maldonado, and N. M. Price. 1996. The role of heterotrophic bacteria in iron-limited ocean ecosystems. Nature 383:330-332[CrossRef]. |
| 41. | Tortell, P. D., M. T. Maldonado, J. Granger, and N. M. Price. 1999. Marine bacteria and biogeochemical cycling of iron in the oceans. FEMS Microbiol. Ecol. 29:1-11. |
| 42. |
Weiburg, W. G.,
S. M. Barns,
D. A. Pelletier, and D. J. Lane.
1991.
16S ribosomal DNA amplification for phylogenetic study.
J. Bacteriol.
173:697-703 |
| 43. | Winkelmann, G., D. van der Helm, and J. B. Neilands (ed.). 1987. Iron transport in microbes, plants and animals. VHC Press, Weinheim, Germany. |
| 44. | Wu, J., and G. W. Luther, III. 1995. Complexation of Fe(III) by natural organic ligands in the northwest Atlantic Ocean by a competitive ligand equilibration method and a kinetic approach. Mar. Chem. 50:159-177. |
| 45. | Yoshinaga, I., K. Katanozaka, and Y. Ueno. 1999. VBNC (viable but nonculturable) marine bacteria on the molecular biological aspects. Microbes Environ. 14:123-129. |
| 46. | Zhang, L., P. J. Murphy, A. Kerr, and M. E. Tate. 1993. Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones. Nature 362:446-448[CrossRef][Medline]. |
| 47. |
Zhu, J.,
J. W. Beaber,
M. I. More,
C. Fuqua,
A. Eberhard, and S. C. Winans.
1998.
Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the TraR protein of Agrobacterium tumefaciens.
J. Bacteriol.
180:5398-5405 |
Applied and Environmental Microbiology, July 2000, p. 2797-2803, Vol. 66, No. 7
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