European Review for Medical and Pharmacological Sciences
Screening of extracts of algae from
Baja California Sur, Mexico as reversers of
the antibiotic resistance of some
pathogenic bacteria
M. MUÑOZ-OCHOA, J.I. MURILLO-ÁLVAREZ, L.A. ZERMEÑO-CERVANTES,
S. MARTÍNEZ-DIAZ, R. RODRÍGUEZ-RIOSMENA*
Departamento de Desarrollo de Tecnologías, Centro Interdisciplinario de Ciencias Marinas,
Instituto Politécnico Nacional, La Paz (Mexico);
*Departamento de Biología Marina, Universidad Autónoma de Baja California Sur,
La Paz (Mexico)
Abstract. – Background and Objec-
tives: Sixty ethanol extracts of marine flora of
Baja California Sur (Mexico) were screened to
evaluate the reversing effect of the bacterial re-
sistance to antibiotics in combination with a
sublethal concentration of ampicillin or ery-
thromycin.
Materials and Methods: The activity was as-
sayed by using a modification of the classical
agar-diffusion method against 3 resistant, patho-
genic bacteria; Escherichia coli (ATCC BAA196),
Staphylococcus aureus (ATCC BAA42), and
Streptococcus pyogenes (ATCC BAA946).
Results: From the 60 ethanolic extracts, 12
(20%) of them in combination with ampicillin
were able to reverse the resistance of Staphylo-
coccus aureus and 8 (13%) with erythromycin
yielded the same reversal with Streptococcus
pyogenes. An extract from Sargassum horridum
was the only one that reversed the resistance to
antibiotics against both Staphylococcus aureus
and Streptococcus pyogenes.
Conclusions: Our findings suggest that
some algae may be source of compounds with
the potential to reverse the antibiotic resis-
tance of some bacteria. In addition, of the as-
sayed extracts, 35 (57%) showed inhibitory ac-
tivity against Staphylococcus aureus, 48 (78%)
were active against Streptococcus pyogenes,
but none was active against Escherichia coli.
The most active extracts were from Laurencia
spp., Gelidium robustum, Chnoospora implexa,
Padina mexicana, Gracilaria subsecundata, and
Dictyopteris undulata.
Key Words:
Escherichia coli, Streptococcus, Staphylococcus,
Antimicrobial.
Corresponding Author: Mauricio Muñoz-Ochoa, MD; e-mail: mmo6709@gmail.com
2010; 14: 739-747
Introduction
Today, an increasing demand of new com-
pounds to combat the bacterial resistance to an-
tibiotics is globally recognized. Resistance is a
phenomenon characterized by having serious
health and socioeconomic implications. Because
of the bacterial resistance, a number of infec-
tious diseases are becoming difficult to treat,
making it necessary to be more aggressive and
using expensive treatments over a longer time1.
The problem is global, complex, and includes a
large number of bacteria of pathological impor-
tance. The multicausality of the resistance
makes it a difficult problem with which to deal2.
Highly populated areas, inadequate control of
infections, and the transference of patients be-
tween hospitals are important factors causing the
increasing of the resistance. The changes in the
ecology of infections observed since the intro-
duction of the antimicrobial agents have been
well-documented2. In response to those changes,
bacteria have developed a number of adaptive
strategies; enzyme inactivation, efflux pumps,
target alteration, and permeability changes3,4. The
most successful mechanisms of resistance are the
expression of enzymes able to degrade the β-lac-
tam ring of penicillins and cephalosporins5 and
efflux pumps that are able to extrude structurally
diverse compounds, including antibiotics, from
the cell. To combat the rapid spread of bacteria
expressing resistance, many Authors5-8 agree for
the need to discover new antibacterials and resis-
tance-reversing agents. This latter involves the
739
M. Muñoz-Ochoa, J.I. Murillo-Álvarez, L.A. Zermeño-Cervantes, S. Martínez-Diaz, R. Rodríguez-Riosmena
discovery of compounds able to inhibit those
mechanisms that confer resistance to antibiotics
by the bacteria. With this in mind, in our research
a library of extracts from marine macroalgae
from Mexico were screened as reversers of the
resistance to antibiotics of three pathogenic bac-
teria to select unexplored sources of resistance-
reversing compounds. This choice is justified be-
cause marine algae are important sources of
metabolites, such as acetogenins, polyphenolics,
aromatic compounds, terpenes, and other related
structures9. To the best of our knowledge this is
the first time in which marine macroalgae col-
lected from the coasts of Baja California Sur,
Mexico have been assessed as reversers of the re-
sistance to antibiotics. Our finding has allowed
us to select a number of algae for further investi-
gation in search for the active compounds.
Materials and Methods
The algae studied were gathered from several
locations along the coast of Baja California Sur
(Figure 1) between June 2004 and November
2007. The collection was done by free diving at
1- to 2-m depth. Algal samples were cleaned of
epiphytes, rinsed with tap water to remove any
associated debris, and the cleaned fresh materials
were dried in the sun, ground, and stored at
–20°C until extraction. Voucher specimens were
preserved for taxonomic identification and future
reference.
The extracts were obtained by maceration.
Briefly, 100 g of each algal sample was soaked
with 250 mL of distilled ethanol at 25-35°C. Af-
ter 48 h, the mixture was filtered through paper.
The residual algal tissue was extracted once
again under same conditions. After filtration,
both extracts were pooled and concentrated to
dryness under vacuum at 40°C (Yamato RE500,
San Francisco, CA, USA). The crude extracts
were kept in dark and dry conditions at –20°C
until biological testing.
A modification of the classical agar disc-diffu-
sion method10 was used to test the effect of ex-
tracts on the reversion of the resistance of Es-
cherichia coli (ATCC BAA-196, expressing ex-
tended spectrum β-lactamases), Staphylococcus
aureus (ATCC BAA-42, β-lactamases), and
Streptococcus pyogenes (ATCC BAA-946, efflux
pump). Each strain was first cultured on Mueller-
Hinton agar plates at 37°C. After 18 h, the cell
740
biomass was harvested and suspended in a 0.85%
sodium chloride solution. The cell density was
adjusted by spectrophotometry (Merck SQ118,
Darmstadt, Germany) at λ 585 nm until 1.0 AU
(equivalent to 4.5 × 107 cells mL-1). The suspen-
sions of each strain were used to inoculate the
surface of Mueller-Hinton agar plates with an
added sublethal concentration of an antibiotic.
Escherichia coli and Staphylococcus aureus were
cultured on Mueller-Hinton agar with added
ampicillin (12 mg L-1, equivalent to 75% of the
minimum inhibitory concentration (MIC)). The
medium for Streptococcus pyogenes was added
erythromycin (1.5 mg L-1, equivalent to 25% of
the MIC). The drug susceptibility pattern of
each target strain was previously determined.
The culturing conditions of strains under sub-
lethal concentrations of antibiotic were exten-
sively tested and optimized. The assays were
done by putting, on the inoculated surface of the
agar plate, extract-impregnated paper discs (6.5
diameter, Whathman No. 4). Each paper disc
was loaded with 100 µL of a stock solution of
each algal extract (20 mg mL-1). The impregna-
tion of the disc was done under aseptic condi-
tions. Solvent evaporation from the discs left
2.0 mg disc-1. Plates were incubated at 37°C.
The inhibition zone (when observed) around
discs was measured after 24 h, and expressed in
mm. Every algal extract was tested in a medium
added with antibiotic (as mentioned before) and
its effect was contrasted by testing the same ex-
tract, at the same time, in Mueller-Hinton agar
without an antibiotic. Those extracts active
against bacteria cultured on a medium with
added antibiotic, but inactive in an antibiotic-
free medium were considered as reversers of the
resistance. Measures of the inhibition zones are
presented as the mean values of two measure-
ments and its SD. Ethanol was always used as a
negative control.
Statistical Analysis
We have found a great difficult to perform a
statistical analysis. However, we have taken into
mind that:
• The substances produced by each alga do not
necessarily correspond to the same chemical
group as well as we cannot assume that they
are in the same concentration, therefore a
comparison between them we could give an
erroneous interpretation of the activity of each
of the species.
 Reversion of the antibiotic resistance

Figure 1. Map of Baja California peninsula (Mexico) showing the different collection locations.

• The effect of each alga on the three test bacte-
ria cannot be compared because the mecha-
nisms used by bacteria to resist antibiotics are
different (β-lactamases and efflux pump as
mentioned in the introduction). Thus although
in some cases there is a tendency to increase
the diameter of the halos when the algae ex-
tract is placed in the presence of the antibiotic,
it cannot be directly interpreted as an effect of
inhibition of antibiotic resistance, because the

741
M. Muñoz-Ochoa, J.I. Murillo-Álvarez, L.A. Zermeño-Cervantes, S. Martínez-Diaz, R. Rodríguez-Riosmena
extract has antibacterial activity and therefore
both mechanisms may be acting simultaneous-
ly. In future work, surely we must focus to de-
scribe the nature of the compounds responsi-
ble for the antibacterial activity and effect of
each of the molecules in the presence of an-
tibiotics.
• Therefore we consider the only valid criterion
to define some attribute the extracts was attrib-
utable to the presence of antibiotic that inhibi-
tion is present whereas in the absence of an-
tibiotic inhibition was not observed. With the
foregoing, we dismiss the ability of the ex-
tracts per se to inhibit the process of bacterial
resistance to antibiotics. In this case the values
were zero for the diameter of halo in the ab-
sence of antibiotic and values of 8 mm or
more for the diameter of halo in the presence
of antibiotic.
Results
As seem in Table I, from all the 60 algal ex-
tracts assessed, 9 extracts, 15%, were able to re-
verse the resistance of Staphylococcus aureus to
a sublethal concentration of ampicillin. The ef-
fect was denoted by the inhibition of growth in
combination of the antibiotic and extracts from
Padina crispata (sample ID: 04-002), Hypnea
valentiae (04-011), Sargassum horridum (04-
003), Rosenvingea. intricata (04-015), Spyridia
filamentosa (04-025), Liagora californica (06-
008), Chondracanthus canaliculatus (07-010),
Codium amplivesiculathum (04-004) and Codi-
um cuneatum (06-011). The extracts from Sar-
gassum horridum (04-003), Cystoseira os-
mundacea (06-023), Chondracanthus canalicu-
latus (06-026), Hypnea johnstonii (06-035),
Pterosiphonia bipinnata (07-003), Spyridia fila-
mentosa (07-006), Gracilaria marcialana (07-
007), and Colpomenia sinuosa (07-008) showed
the same effect on the resistance of Streptococ-
cus pyogenes to erythromycin. From the 3 tested
extracts of Sargassum horridum collected in dif-
ferent years, just the extract from the specimen
04-003 was active. In addition, Sargassum hor-
ridum (04-003) was the one that showed a re-
verser effect on the antibiotic resistance of
Staphylococcus aureus and Streptococcus pyo-
genes against ampicillin and erythromycin. Sur-
prisingly, none of extracts tested was able to af-
fect the growth of Escherichia coli.
742
Discussion
Objective of this study was to evaluate the
ability of extracts of marine algal species collect-
ed from several locations from Baja California
Sur (Mexico) to inhibit (or reverse) the mecha-
nism of resistance to antibiotics of three patho-
genic bacteria.
In the literature there are numerous reports
about a broad range of antimicrobial activities
from algal extracts from around the world11-20, in-
cluding algae from Mexican waters21-2. A number
of algal natural products with antimicrobial ac-
tivity have been described in the past few
decades9. After an extensive bibliographic review
through electronic data bases, reports of a revers-
er effect of the algal extracts on antibiotic-resis-
tance of bacteria were not found. Probably our
study is a pioneer in this area.
As mentioned, just those extracts that were ac-
tive against bacteria cultured in a medium with
an added sublethal concentration of antibiotic
(but necessarily an extract inactive by itself) were
considered as inhibitors of the mechanisms of
bacterial resistance. That interpretation was done
under the assumption of that some compounds
present in the extracts were able to inhibit the β-
lactamase activity in Staphylococcus aureus and-
or the efflux pump in Streptococcus pyogenes al-
lowing the added antibiotic (ampicillin or ery-
thromycin) to cause cell growth inhibition, de-
noted by inhibition zones around the discs.
In the search for inhibitors of the mechanisms
of bacterial resistance, inhibitors have been found
mainly in bacteria or by chemical synthesis. For
example, the clavulanic acid produced by Strepto-
myces clavuligerus acts as an inhibitor of β-lacta-
mases, which are a defensive response to the β-
lactam antibiotics25. Competitive inhibition is the
mode of action of the clavulanic acid caused by a
structure identical to the natural β-lactamase sub-
strate. We believe that competitive inhibitors of β-
lactamases can be found in macroalgae and that is
our explanation for the observed effect of Sargas-
sum horridum (04-003) on the resistance of
Staphylococcus aureus against ampicillin. This
idea is supported by the isolation of sargassum-
lactam from Sargassum kjellmanianum26. Consid-
ering that similar compounds may be synthesized
by other brown algae, the effect shown by Padina
crispata (04-002) and Rosenvingea intricata (04-
015) on the resistance of Staphylococcus aureus
may be explained by the presence of structures
similar to the sargassumlactam.
 Table I. Diameter of inhibition zone around the discs individually impregnated with sixty algal extracts collected from Baja California Sur (Mexico). Bacteria were cultured on
Mueller Hinton agar plates add with a sublethal concentration of antibiotic.

Diameter of the inhibition zone, in mma

S. aureus S. pyogenes E. coli
MAWA CWA MAWE CWA MAWA CWA

Family
Sample ID, species name, and authority (collection place)

Bangiaceae
06-020, Porphyra perforata Agardh, 1883 (2) 0±0 0±0 0±0 0±0 0±0 0±0

Chnoosporaceae
04-018, Chnoospora implexa Agardh, 1848 (8) 10.0 ± 0 7.0 ± 0 19.5 ± 07 12.0 ± 0 0±0 0±0

Cladophoraceae
06-001, Cladophora sp. (7) 10.0 ± 1.4 7.0 ± 0 16.0 ± 1.4 22.0 ± 1.4 0±0 0±0

Codiaceae
04-004, Codium amplivesiculatum Setchell & Gardner, 1924 (8) 8.0 ± 0 0±0 13.0 ± 0 12.0 ± 0 0±0 0±0(
06-012, Codium amplivesiculatum Setchell & Gardner, 1924 (6) 0±0 0±0 11.5 ± 0.7 10.0 ± 0±0 0±0
04-024, Codium cuneatum Setchell & Gardner, 1924 (8) 10.0 ± 0 9.5 ± 0.7 14.5 ± 0.7 11.0 ± 0 0±0 0±0
06-011, Codium cuneatum Setchell & Gardner, 1924 (6) 9.5 ± 2.1 0±0 15.0 ± 0 12.5 ± 0.7 0±0 0±0
06-010, Codium simulans Setchell & Gardner, 1924 (6) 9.5 ± 0.7 7.0 ± 0 11.5 ± 0.7 8.0 ± 0 0±0 0±0

Corallinaceae
07-001, Amphiroa valonioides Yendo, 1902 (7) 0±0 0±0 11.0 ± 0 17.5 ± 2.1 0±0 0±0
06-025, Corallina vancouveriensis Yendo, 1902 (4) 9±0 11.0 ±0 9.5 ± 0.7 13.5 ± 0.7 0±0 0±0
06-027, Corallina sp. (2) 15.5 ± 0.7 9.5 ± 0.7 15.5 ± 0.7 10.5 ± 0.7 0±0 0±0
Reversion of the antibiotic resistance

Cystocloniaceae
06-035, Hypnea johnstonii Setchell & Gardner, 1924 (2) 0±0 7.0 ± 0 10.0 ± 0 0±0 0±0 0±0
04-011, Hypnea valentiae (Turner) Montagne, 1841 (8) 8.0 ± 0 0±0 12.5 ± 0.7 10.5 ± 0.7 0±0 0±0

Dictyotaceae
06-016, Dictyota flabellata Setchell & Gardner, 1924 (6) 10.0 ± 0 7.5 ± 0.7 14.0 ± 0 18.5 ± 0.7 0±0 0±0
06-028, Dictyopteris undulata Holmes, 1896 (2) 18.0 ± 0 14.0 ± 1.4 21.5 ± 0.7 18.5 ± 0.7 0±0 0±0
06-029, Dictyopteris delicatula Lamouroux, 1809 (2) 14.5 ± 0.7 11.5 ± 1.4 13.0 ± 1.4 11.0 ± 0 0±0 0±0
04-002, Padina mexicana Thivy, 1945 (8) 9.5 ± 0.7 0±0 11.0 ± 0 10.0 ± 0 0±0 0±0
04-021, Padina mexicana Thivy, 1945 (8) 14.5 ± 0.7 7.0 ± 0 16.5 ± 0.7 10.0 ± 0 0±0 0±0
06-018, Padina concrescens Thivy, 1945 (2) 10.5 ± 0.7 7.0 ± 0 12.5 ± 0.7 11.0 ± 0.7 0±0 0±0

743
(Continued)
744
Table I. Diameter of inhibition zone around the discs individually impregnated with sixty algal extracts collected from Baja California Sur (Mexico). Bacteria were cultured on
Mueller Hinton agar plates add with a sublethal concentration of antibiotic.

Diameter of the inhibition zone, in mma

S. aureus S. pyogenes E. coli
MAWA CWA MAWE CWA MAWA CWA

Gelidiaceae
04-008, Gelidium robustum Hollenberg & Abbott, 1965 (3) 11.0 ± 1.4 11.5 ± 0.7 22.5 ± 0.7 19.0 ± 0 0±0 0±0
06-024, Gelidium robustum Hollenberg & Abbott, 1965 (4) 14.0 ± 1.4 8.5 ± 0.7 14.0 ± 1.4 7.0 ± 0 0±0 0±0
06-033, Gelidium robustum Hollenberg & Abbott, 1965 (2) 12.5 ± 2.1 10.5 ± 0.7 14.5 ± 0.7 11.0 ± 0.7 0±0 0±0

Gigartinaceae
06-026, Chondracanthus canaliculatus Harvey, 1993 (2) 9.5 ± 0.7 7.5 ± 0.7 10.0 ± 1.4 0±0 0±0 0±0
07-010, Chondracanthus canaliculatus Harvey, 1993 (1) 9.0 ± 0 0±0 0±0 0±0 0±0 0±0

Gracilariaceae
07-007, Gracilaria marcialana Setchell & Gardner, 1924 (8) 0±0 0±0 11.0 ± 0 0±0 0±0 0±0
04-007, Gracilaria veleroae Dawson, 1944 (8) 0±0 0±0 0±0 0±0 0±0 0±0
04-010, Gracilaria vermiculophylla (Ohmi) Papenfuss, 1967 (5) 0±0 0±0 11.0 ± 0 11.0 ± 0 0±0 0±0
04-023, Gracilaria subsecundata Setchell & Gardner, 1924 (8) 13.5 ± 0.7 11.0 ± 1.4 14.0 ± 0 9.0 ± 1.4 0±0 0±0

Laminariaceae
06-019, Macrocystis pyrifera Agardh, 1820 (2) 9.0 ± 0 10.0 ± 0 11.0 ± 0 18.5 ± 0.7 0±0 0±0

Lessoniaceae
06-022, Eisenia arborea Areschoug, 1876 (2) 0±0 0±0 0±0 0±0 0±0 0±0

Liagoraceae
04-022, Ganonema farinosum Fan & Wang, 1974 (8) 12.5 ± 2.1 9.0 ± 0 17.0 ± 2.1 17.0 ± 0 0±0 0±0
06-008, Liagora californica Zeh, 1912 (8) 9.0 ± 0 0±0 13.5 ± 1.4 10.5 ± 0.7 0±0 0±0
06-013, Liagora californica Zeh, 1912 (6) 0±0 0±0 0±0 0±0 0±0 0±0

Rhodymeniaceae
06-003, Rhodymenia californica Kylin, 1931 (7) 7.0 ± 0 7.0 ± 0 14.0 ± 0 13.0 ± 0 0±0 0±0
06-032, Rhodymenia californica Kylin, 1931 (2) 0±0 0±0 0±0 0±0 0±0 0±0

(Continued)
M. Muñoz-Ochoa, J.I. Murillo-Álvarez, L.A. Zermeño-Cervantes, S. Martínez-Diaz, R. Rodríguez-Riosmena
 Table I. Diameter of inhibition zone around the discs individually impregnated with sixty algal extracts collected from Baja California Sur (Mexico). Bacteria were cultured on
Mueller Hinton agar plates add with a sublethal concentration of antibiotic.

Diameter of the inhibition zone, in mma

S. aureus S. pyogenes E. coli
MAWA CWA MAWE CWA MAWA CWA

Rhodomelaceae
07-004, Acanthophora spicifera (M. Vahl) Børgesen, 1910 (8) 0±0 0±0 12.0 ± 0 10.5 ± 0.7 0±0 0±0
07-002, Laurencia gardneri Hollenberg, 1943 (7) 0±0 0±0 10.5 ± 0.7 8.5 ± 0.7 0±0 0±0
04-005, Laurencia johnstonii Setchell & Gardner, 1924 (8) 30.0 ± 0 30.5 ± 0.7 38.0 ± 0.7 26.5 ± 1.4 0±0 0±0
07-009, Laurencia johnstonii Setchell & Gardner, 1924 (8) 12.0 ± 0 11.5 ± 0.7 9.0 ± 1.4 10.5 ± 0.7 0±0 0±0
06-007, Laurencia pacifica Setchell & Gardner, 1924 (8) 19.5 ± 0.7 18.0 ± 0.7 31.5 ± 2.1 25.0 ± 0.7 0±0 0±0
06-015, Laurencia pacifica Setchell & Gardner, 1924 (6) 21.0 ± 0 12.0 ± 0.7 21.5 ± 2.1 19.5 ± 0.7 0±0 0±0
07-005, Laurencia sp. (8) 19.0 ± 0.7 14.5 ± 0.7 30.0 ± 0 30.5 ± 0.7 0±0 0±0
06-031, Neorhodomela larix (Turner) Masuda, 1982 (2) 12.0 ± 1.4 12.0 ± 0 11.0 ± 0 13.0 ± 0 0±0 0±0
07-003, Pterosiphonia bipinnata Falkenberg, 1901 (7) 0±0 0±0 10.5 ± 0.7 0±0 0±0 0±0

Sargassaceae
06-023, Cystoseira osmundacea (Turner) Agardh, 1820 (4) 0±0 0±0 11.0 ± 0.7 0±0 0±0 0±0
04-003, Sargassum horridum Setchell & Gardner, 1924 (8) 9.0 ± 0 0±0 12.0 ± 0 0±0 0±0 0±0
06-005, Sargassum horridum Setchell & Gardner, 1924 (8) 9.0 ± 0.7 7.0 ± 0 13.5 ± 0.7 14.0 ± 1.4 0±0 0±0
06-009, Sargassum horridum Setchell & Gardner, 1924 (8) 9.5 ± 0.7 7.0 ± 0 15.5 ± 0.7 14.5 ± 0.7 0±0 0±0

Scytosiphonaceae
04-017, Hydroclathrus clathratus (Agardh) Howe, 1920 (8) 10.5 ± 0.7 7.0 ± 0 13.0 ± 0 12.0 ± 0 0±0 0±0
06-006, Hydroclathrus clathratus (Agardh) Howe, 1920 (8) 9.5 ± 0.7 7.0 ± 0 12.5 ± 0.7 15.0 ± 0 0±0 0±0
04-015, Rosenvingea intricata (Agardh) Børgesen, 1914 (8) 11.5 ± 0.7 0±0 15.0 ± 0 10.0 ± 0 0±0 0±0
04-020, Rosenvingea intricata (Agardh) Børgesen, 1914 (8) 7.5 ± 0.7 7.0 ± 0 13.0 ± 0.7 13.0 ± 0 0±0 0±0
Reversion of the antibiotic resistance

06-004, Rosenvingea intricata (Agardh) Børgesen, 1914 (8) 9.0 ± 0 7.0 ± 0 14.0 ± 0 11.5 ± 0.7 0±0 0±0
06-017, Colpomenia tuberculata Saunders, 1898 (6) 10.5 ± 2.1 8.0 ± 0 20.5 ± 13.4 9.5 ± 0.7 0±0 0±0
06-030, Colpomenia tuberculata Saunders, 1898 (2) 13 ± 1.4 13 ± 0 13 ± 0 10 ± 0 0±0 0±0
07-008, Colpomenia sinuosa Derbés & Solier, 1851 (8) 11.0 ± 0 9.0 ± 0 10.5 ± 0.7 0±0 0±0 0±0

Spyridiaceae
04-025, Spyridia filamentosa (Wulfen) Harvey, 1833 (5) 10.5 ± 0.7 0±0 15.0 ± 0 7.0 ± 0 0±0 0±0
07-006, Spyridia filamentosa (Wulfen) Harvey, 1833 (5) 11.0 ± 0 9.0 ± 0 11.5 ± 0.7 0±0 0±0 0±0

Ulvaceae
04-001, Ulva rigida Agardh, 1823 (8) 0±0 0±0 15 ± 0 7.0 ± 0 0±0 0±0
06-002, Ulva dactylifera Setchell & Gardner, 1920 (7) 11.0 ± 0.7 7.0 ± 0 14.5 ± 0.7 11.0 ± 0 0±0 0±0

a
Mean values (n = 2) ± standard deviation. MAWA = cultured on medium added with 75% of the MIC of ampicillin; CWA = cultured without antibiotic; MAWE = cultured on

745
medium added with 25% of the MIC of erythromycin.
M. Muñoz-Ochoa, J.I. Murillo-Álvarez, L.A. Zermeño-Cervantes, S. Martínez-Diaz, R. Rodríguez-Riosmena
The synthetic inhibitors of a bacterial efflux
pump have been investigated in the activity of the
NorA pump expressed in some species of the
genus Staphylococcus and Streptococcus 27,28.
Among the compounds investigated as pump in-
hibitors are the indole alkaloid reserpine, and
some tyrosine derivatives such as MC207110 and
INF240. Other compounds containing bro-
mophenol as structural moieties have been inves-
tigated29,28. The literature shows that compounds
related to those inhibitors of the NorA pump are
present in extracts from Hypnea johnstonii (06-
035), Chondracanthus canaliculatus (06-026),
Gracilaria marcialana (07-007), Pterosiphonia.
bipinnata (07-003), Colpomenia osmundacea
(06-023), Sargassum horridum (04-003),
Colpomenia sinuosa (07-008), and Spyridia fila-
mentosa (07-006)9, and we believe that may ex-
plain the effect observed by the extracts on the
resistance of Streptococcus pyogenes.
In this study, a different response was mea-
sured by extracts from same species collected in
different locations and-or year. Temporal and
spatial variation of the biological responses of
crude extracts of marine organisms as a conse-
quence of biotic and nonbiotic conditions has
been extensively documented30-34.
One can note that 80% of the extracts were ac-
tive against one, and 51% were active against
two target organisms.
Conclusions
The results clearly suggest that macroalgae
collected from Baja California Sur (Mexico) are
an interesting resource for the search for com-
pounds that may be developed as potential re-
versers of some mechanisms of bacterial resis-
tance to antibiotics. The finding of new reversers
of resistance may have important implications
for public health.
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––––––––––––––––––––
Acknowledgements
This study was done in partial fulfillment of the require-
ments of a Doctor in Sciences degree for MMO, with
grants from IPN (ref. SIP 20070020, SIP 20080216),
and CONACyT (ref. SEP-47942/A-1). Stephanie Castro
is acknowledged for technical assistance during the ex-
tractions. Authors thank COFAA-IPN and EDI-IPN for
the incentives granted. Thanks also to Dr. Ellis Glazier
for editing this English-language text.
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