SciELO - Scientific Electronic Library Online

 
vol.36 número1INCREMENTO DE NITRÓGENO EN Thalassia testudinum POR EL APORTE DE NITRÓGENO DISUELTO INORGÁNICO DE AGUAS RESIDUALES DURANTE PRECIPITACIONES EXTRAORDINARIAS índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados

Revista

Articulo

Indicadores

Links relacionados

  • No hay artículos similaresSimilares en SciELO

Compartir


Revista internacional de contaminación ambiental

versión impresa ISSN 0188-4999

Rev. Int. Contam. Ambient vol.36 no.1 Ciudad de México feb. 2020  Epub 22-Dic-2020

https://doi.org/10.20937/rica.2020.36.53432 

Short communications

BACTERIAL MICROBIOTA FROM WILD FRESHWATER FISH UTILIZED FOR SUBSISTENCE IN WESTERN MEXICO

MICROBIOTA BACTERIANA DE PECES SILVESTRES DE AGUA DULCE UTILIZADOS PARA CONSUMO EN EL OESTE DE MÉXICO

Rosa Leonor González-Díaz1 

Norman Mercado-Silva2  * 

Eire Reynaga-Delgado3 

Luis Manuel Martínez-Rivera1 

1Departamento de Ecología y Recursos Naturales, Centro Universitario de la Costa Sur (CUCSUR). Universidad de Guadalajara. Av. Independencia Nacional #151 C.P. 48900, Autlán de Navarro, Jalisco, C.P. México

2Centro de Investigación en Biodiversidad y Conservación, Universidad Autónoma del Estado de Morelos. Av. Universidad #1001. C.P: 62210. Col. Chamilpa, Cuernavaca, Morelos, México

3Centro Universitario de Ciencias Exactas e Ingeniería (CUCEI). Universidad de Guadalajara. Blvd. Marcelino García Barragán # 1421, C.P. 444430, Guadalajara, Jalisco, México


ABSTRACT

Microbiological analyses of freshwater fish utilized in subsistence fisheries are relatively scarce. These fisheries are widespread throughout Latin America, and support numerous communities in rural, impoverished areas. We present the results of genetically-based microbiological analyses of river water samples and fish tissue samples obtained from specimens (n = 128) captured in the wild from three sites in the Ayuquila river, west central Mexico. The system is affected by numerous human activities. We identify 11 bacterial taxa of which Pseudomonas stutzeri, Shigella sonnei, Escherichia coli and Bacillus subtilis were isolated from the most fish. Citrobacter freundii and E. coli were present in water samples from all sites. Average taxa richness was similar among rainy and dry seasons. Enterobacteriaceae dominate the bacterial microbiota of water and fishes of the Ayuquila river, suggesting there is significant influence from anthropic activities in the basin. Our findings provide a baseline upon which to improve our understanding of the microbiology of the Ayuquila river and similar systems in west central Mexico, especially related to risks for biota and human populations dependent on rivers for sustenance.

Key words: Escherichia coli; urban pollution; Manantlán; subsistence fishery

RESUMEN

Los análisis microbiológicos en peces de agua dulce tomados directamente de hábitats naturales y que son utilizados en pesquerías de subsistencia son relativamente escasos. Estas pesquerías están muy extendidas en toda América Latina y son importantes para numerosas comunidades en áreas rurales empobrecidas. Presentamos los resultados de análisis microbiológicos y moleculares realizados en muestras de agua de río y muestras de tejido obtenidas de peces (n = 128) capturados en el medio silvestre de tres sitios en el río Ayuquila, en el centro oeste de México. El río es afectado por numerosas actividades humanas. Identificamos 11 taxa bacterianos de los cuales Pseudomonas stutzeri, Shigella sonnei, Escherichia coli y Bacillus subtilis se aislaron de la mayoría de los peces. Citrobacter freundii y E. coli estuvieron presentes en muestras de agua de todos los sitios. La riqueza promedio de los taxa fue similar entre temporadas de muestreo. Las enterobacteriáceas dominan la microbiota bacteriana del agua y los peces del río Ayuquila, lo que sugiere que existe una influencia significativa de las actividades antrópicas en la cuenca. Nuestros resultados proporcionan la línea base sobre la cual mejorar nuestra comprensión de la microbiología del río Ayuquila, especialmente relacionada con los riesgos para la biota y las poblaciones humanas que dependen y subsisten del río.

Palabras clave: Escherichia coli; contaminación; Manantlán; pesquería de subsistencia

INTRODUCTION

An important proportion of the rural population in Mexico relies on subsistence riverine fisheries for protein intake (Periago et al. 2005, Rincón-Rodríguez et al. 2013, Urquía-Fernández 2014). Subsistence fisheries usually complement agriculture and cattle rearing as main sources of food and wealth in many watersheds in west central Mexico (Elías-Fernández and Navarrete-Salgado 1998, Lyons et al. 1998). Unfortunately, rivers in this area suffer from multiple human stressors, including organic urban and agricultural pollution (Hernández-Antonio and Hansen 2011, Torres-Beristáin et al. 2013). Freshwater fisheries in the Ayuquila-Armería river (hereafter the Ayuquila river) in the states of Jalisco and Colima, Mexico, have experienced important declines but remain a key resource for the local population (Lyons et al. 1998, Mercado-Silva et al. 2011). The Ayuquila river has long been locally known for the quality of its fishery and as a biodiversity hotspot (Lyons et al. 1998, Arellano-Ríos and Rivera-Pahua 2011). However, agricultural activities and urban development have negatively affected various segments of the river. Importantly, urban centers with populations of > 40 000 people dispose of untreated wastewaters directly onto channels connected to the river and little control exists for disposing of feces from > 20 000 cattle in the basin (Graf-Montero et al. 2006). Such high levels of organic pollutants in the Ayuquila river represent a potential microbiological hazard for humans utilizing river resources.

Microbiological analyses of freshwater fish utilized in subsistence fisheries are relatively rare; most microbiological information to date comes from fish farms, aquaculture, and canning operations (Lyhs et al. 2001, Arvanitoyannis et al. 2008), but little is known about wild fish microbiota and how environmental conditions of rivers affect their microbial diversity (Lazado et al. 2015). Information is also scarce in Mexico about the potential health risks pathogenic bacteria from wild freshwater fish pose to fish handlers and consumers, especially when fish come from systems affected by urban or agricultural wastewaters (Cahill 1990). Here we present the results of genetically-based microbiological analyses of water and tissue samples obtained from fish specimens captured in the wild in three different Ayuquila river sections exposed to differential wastewater loads. We describe differences among sections and draw conclusions that should alert local health officials about the potential for health risks to humans in the basin.

MATERIAL AND METHODS

Study sites

The Ayuquila river is located in western Mexico, in the northwestern portion of the Sierra Madre del Sur ~50 km inland from the Pacific Ocean (Fig. 1). The Ayuquila runs along a series of gorges and valleys and has a total length of approximately 294 km. Urban centers and agricultural activities are concentrated in the valleys. The river is important from a conservation perspective, as it is the northern boundary of the Sierra de Manantlán Biosphere Reserve (SMBR). The SMBR is a protected area dedicated to biological conservation where low impact human activities are permitted, and where some human populations still rely on natural resource use and consumption (Graf-Montero et al. 2006). Fishing is an important activity for humans inside the SMBR, in particular those living in the margins of the Ayuquila (Mercado-Silva et al. 2011). This study focuses on a ~20 km segment of the Ayuquila that runs from the town of El Corcovado, ~1 km upstream from the valley of the cities of Autlán and El Grullo, through the valley, to a section of river located upstream from where the river becomes part of the SMBR boundary. Prior to entering the valley, the river flows through a gorge with little human influence; as it runs through the valley and before entering the SMBR the river receives numerous canals carrying municipal and agricultural wastewater (Fig. 1). Within the river segment, fish and water samples were collected from three sites: (1) Corcovado, (2) Pablo Blanco and (3) Achacales. Site 1 was located just downstream (2 km) from the gorge in a section with comparatively little human influence, site 2 was located just downstream (0.5 km) from where municipal wastewater canals empty into the river, and site 3 was located about 1.5 km downstream from site 2, as the river enters the SMBR (Fig. 1). Fishing activities have been recorded from all three sites (Mercado-Silva et al. 2011). Water physical-chemical parameters (obtained with a Hanna 9828 multimeter in triplicate in each sampling event) varied from site to site and among wet (July-October) and dry (November-June) seasons at the time of sampling (Table I).

Fig. 1 Three sampling sites in Ayuquila river (west central Mexico) (black line). Cities of Autlán and El Grullo, and the main outlet for their sewage systems are shown (white lines) Coordinates in UTM (zone 13Q). The inset shows a map of the State of Jalisco, and the location of the study area 

TABLE I PHYSICAL CHEMICAL PARAMETERS (AVERAGE) FROM WATER IN THREE (1-3) SITES (SEE METHODS FOR SITE DESCRIPTION) AND TWO SEASONS (WET = W; DRY = D) IN THE AYUQUILA RIVER, WEST CENTRAL MEXICO. 

Season Site 1 Site 2 Site 3
W D W D W D
Temperature (º Celsius) 20.3 18.9 23.8 22.6 22.7 21.8
pH 8.26 7.75 7.60 7.40 7.90 8.48
Dissolved oxygen (mg/L) 5.70 5.90 2.98 2.10 2.09 4.90
Conductivity (µS/cm) 97.5 151.0 449.3 517.5 226.5 532.0
Total dissolved solids (ppm) 49.0 75.5 224.0 259.0 113.0 266.0
Salinity (ppt) 0.04 0.07 0.21 0.25 0.11 0.26

Sampling

Water and fish samples were obtained diurnally during 2015 in February, March and April (dry season) and in July, September and October (wet season), from each site. Fish (n = 128) were collected using traditional fishing methods (e.g., cast netting) and kept alive in river water as they were transported to the laboratory (Centro Universitario de la Costa Sur, Universidad de Guadalajara in Autlán, Jalisco, Mexico). Tilapia (Oreochromis sp.), bluegill (Lepomis macrochirus), carp (Cyprinus carpio) and goldfish (Carassius auratus), all non-native fishes, were collected. Tilapia comprised the majority of examined fish (95 %); we do not examine microbiological differences among species. Fish were sacrificed within 24 hours of their capture, measured, weighed and dissected to obtain a 10 g tissue sample comprising a mix of intestine, branchiae, liver, muscle and eggs (when available). The sample was then preserved in 90 mL of enriched peptone water.

Water samples were collected using Moore’s swab technique (Barrett et al. 1980). After an hour of contact time with river water, swabs were placed in sterilized glass containers with one of two liquid culture media (peptone water with 0.5 % W/V NaCl and thioglycolate broth). A separate 350 mL sample of river water was obtained in the field. Swabs and water samples were obtained in triplicate at each sampling event; within each site, locations where samples were obtained were all within 20 m from each other. All water samples were transported to the lab in ice chests at a temperature of 4 ºC.

Sample processing

Water and fish tissue samples were planted in culture media to obtain bacterial strains. Media used were thiosulfate-citrate-bile salts-sucrose (TCBS) agar, bismuth sulfite agar, Salmonella-Shigella agar, MacConkey agar and nutritive agar (Bioxon, Mexico). Fish tissue samples were planted in petri dishes with each media. A 1 mL sample from Moore swabs was obtained and planted into separate Petri dishes with media. A 1 mL sample of river water was obtained and planted in culture media upon arrival at the laboratory. Bacterial strains from fish tissue and water samples obtained after 24±2 h incubation were isolated and purified in tryptic soy agar (Becton, Dickinson and Company, France). Twenty three isolates were obtained from both water and fish samples. From each isolate, a subsample was obtained for polymerase chain reaction (PCR) analysis.

Sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS) was used for nucleic acid extraction for each isolated strain (Kabir et al. 2006). Each sample was diluted (1:20), and we used 25 µL for PCR amplification of fD1 and rD1 16S ribosomal genes. PCR products were purified in Bio-Rad chromatography columns (Quantum Prep PCR Kleen Spin columns, Bio-Rad ®). Non-specific bands in chromatography columns were recovered using Promega ® Kit Wizard SV Gel and PCR Clean Up System. Purified products were verified using agarose gel electrophoresis (Lee et al. 2012). Recovered PCR products were sequenced at Macrogen Inc. (Seoul, Korea). Sequences were analyzed using BLAST algorithms from databases at the National Center of Biotechnology Information (NCBI BLAST 2017) and the Kyoto Encyclopedia of Genes and Genome (KEGG 2017).

Using the taxonomic identity of collected bacteria from water samples we compared species presence and species richness (Student t-tests) between sites and between seasons (wet vs. dry). Presence of bacteria isolated from fish tissue samples were also compared among sites and sampling seasons. For bacteria isolated from fish samples, we further analyzed the prevalence (i.e., number of fish containing a certain taxa) among sites and seasons.

RESULTS

We identified 11 taxa of bacteria from water and fish tissue samples from the Ayuquila river (Table II). Isolates from six taxa were identified to genus level only (Alcaligenes sp., Bacillus sp., Methanobacterium sp., Proteus sp., Providencia sp., and Pseudomonas sp.). Species in three of these genera were also identified from isolates (exceptions being Methanobacterium sp. and Alcaligenes sp.). Ten isolates were identified to species level, and only one was identified to subspecies (Table II).

TABLE II BACTERIA IDENTIFIED FROM WATER AND FREE LIVING FRESHWATER FISH SAMPLES FROM THREE (1-3) SITES (SEE METHODS FOR SITE DESCRIPTION) IN THE AYUQUILA RIVER, WEST CENTRAL MEXICO. LIST ORGANIZED ALPHABETICALLY. SAMPLES WERE TAKEN FROM WET (W) AND DRY (D) SEASONS RESPECTIVELY. PRESENCE/ABSENCE IS INDICATED FOR WATER SAMPLES. FOR FISH TISSUE SAMPLES THE NUMBER OF FISH TESTING POSITIVE FOR A TAXON IS INDICATED; THE TOTAL NUMBER OF FISH CAPTURED IN A GIVEN SAMPLING EFFORT IS INDICATED ADJACENT TO D OR W IN COLUMN HEADERS. IN PARENTHESES, THE % OF FISH WHERE A TAXON WAS IDENTIFIED. TOTAL NUMBER OF TAXA IDENTIFIED FROM SAMPLING EVENTS IS PRESENTED (TAXA SUM) 

Sample Source Water Fish
Site 1 2 3 1 2 3
D W D W D W D (19) W (22) D (16) W (17) D (26) W (28)
Species ID
Alcaligenes sp. - 1 - 1 - 1 8 (42.1) 1 (4.5) 1 (6.2) 8 (47.0) 3 (11.5) 11 (39.2)
Bacillus sp. 1 - 1 - 1 - - - 7 (43.7) - 1 (3.8) 1 (3.5)
Bacillus subtilis - - - - - - 6 (31.5) 7 (31.8) 14 (87.5) 8 (47.0) 4 (15.3) 11 (39.2)
B. subtilis inaquosorum - 1 1 1 1 - 5 (26.3) 10 (45.4) 2 (12.5) 7 (41.4) 11 (42.3) 6 (21.4)
Citrobacter freundii 1 1 1 1 1 1 3 (15.8) 1 (4.5) 3 (18.7) 2 (11.7) 8 (30.7) 5 (17.8)
Enterobacter cloaceae - 1 1 - 1 1 - - - - 4 (15.3) 1 (3.5)
Escherichia coli 1 1 1 1 1 1 13 (68.4) 5 (22.7) 4 (25.0) 8 (47.0) 13 (50.0) 14 (50.0)
Methanobacterium sp. 1 1 - - - 1 - 2 (9.0) - - 3 (11.5) 1 (3.5)
Proteus sp. - - 1 - - 1 1 (5.2) 3 (13.6) - 2 (11.7) - 6 (21.4)
Providencia alcalifaciens 1 1 - - 1 1 - - 2 (12.5) - 2 (7.6) 1 (3.5)
Providencia sp. 1 - 1 - 1 1 4 (21.0) - - 4 (23.5) - 7 (25.0)
Pseudomonas fragi 1 - - - 1 - - 5 (22.7) 1 (6.2) 1 (5.8) 1 (3.8) -
Pseudomonas sp. 1 - 1 1 - - 2 (10.5) 4 (18.1) 6 (37.5) 4 (23.5) 7 (26.9) 7 (25.0)
Pseudomonas stutzeri 1 1 1 1 1 - 7 (36.8) 13 (59.0) 12 (75.0) 4 (23.5) 19 (73.0) 9 (32.1)
Serratia liquefaciens 1 1 1 - 1 1 6 (31.5) - - 7 (41.4) - 10 (35.7)
Shigella sonnei 1 - 1 1 1 1 9 (47.3) 13 (59.0) 14 (87.5) 6 (35.2) 13 (50.0) 9 (32.1)
Taxa sum 11 9 11 7 11 10 11 11 11 12 13 15

Most taxa were identified from both water and fish tissue samples. Bacillus subtilis was the only species present in fish tissue samples but absent from water samples. Citrobacter freundii and Escherichia coli were present in water samples from both wet and dry seasons from all sites. Pseudomonas stutzeri, Serratia liquefasciens and Shigella sonnei were recovered from all dry season water samples, but one of them was missing from at least one site sampled during the wet season (Table II). No taxon was exclusive of a site. Average taxa richness was similar among seasons (Student t = 2.64, p = 0.11) but slightly higher richness was observed during the wet season (11-13 in the dry season vs 11-15 in the wet season). Water samples obtained in the wet season from site 2 had the lowest taxa richness.

Five taxa isolated from fish tissue samples were absent from at least one site; Bacillus sp. was absent from site 1, although B. subtilis and B. subtilis inaquosorum were present in the site during both seasons. Enterobacter cloaceae was only present in site 3. Methanobacterium sp. and Providencia alcalifasciens were absent from sites 2 and 1, respectively, but present in other sites during at least one sampling season. Pseudomonas stutzeri and Shigella sonnei were isolated from the most fish (64) across all sites, followed by E. coli (57) and B. subtilis (50). Least prevalent taxa found in fish samples were E. cloaceae, P. alcalifasciens (in five fish only each) and Methanobacterium sp. (in six fish). Site 3 had the highest richness of all sites; all taxa were found in fish captured from the site. Three bacterial taxa -Serratia liquefasciens, Proteus sp. and Providencia sp. - were absent from fish samples in the dry season and only P. fragi was absent from fish samples in the wet season at site 3 (Table II).

Shigella sonnei, P. stutzeri, E. coli and B. subtilis were present in the highest percentage of examined fish tissue samples; S. sonnei and B. subtilis were recovered from 87.5 % of samples from site 2 during the dry season. A high proportion of samples from the dry season in site 2 also tested positive for P. stutzeri. Escherichia coli was identified from a relatively high percentage of fish tissue samples from most sites and seasons; E. coli was recovered from a relatively high proportion of fishes from site 1 in the dry season (68.4 %), and between 20-50 % of all other fishes collected on other sites and seasons were positive for this species (Table II).

DISCUSSION AND CONCLUSIONS

Microbiological information from freshwater systems can help our understanding of biological diversity, the functional role of microorganisms in natural processes (i.e., nutrient cycling), how biota is affected by anthropic stressors, and their interactions with other organisms, including humans (Cahill 1990, Barrera-Escorcia et al. 2013, García-Pérez and Aguilar 2013). These areas of knowledge rely on studies that, as a starting point, identify the suite of species present in the environment or those associated with organisms utilized as resources. Our results provide one of the first accounts of the microbiota from free living fishes in Mexico. Some studies have reported on microbiological conditions of the Gulf of Mexico (Godoy-Lozano et al. 2018) and of river waters in Mexico (Arellano-Ríos and Rivera-Pahua 2011, Barrera-Escorcia et al. 2013), or have analyzed fish destined for consumption in urban markets (Constantino-Casas et al. 1997) but no reports exist on the microbiology of fishes utilized in subsistence fisheries, especially related to natural protected areas.

Our finding that Enterobacteriaceae dominate the bacterial microbiota of water and fishes of the Ayuquila river provides evidence of the influence anthropic impact is having on the river (García-Pérez and Aguilar 2013). This is important both from a public health perspective and considering human effects to aquatic ecosystems in the SMBR. Presence of E. coli, a well-known microbiological water quality indicator, which we found in all sites and in relatively high number of fishes, can be related to constant fecal (animal or human) matter influx to the river (Eckner 1998, Somarelli et al. 2007). Escherichia coli can generate opportunistic pulmonary, gastric and skin infections in humans consuming, swimming or bathing in river waters (Periago et al. 2005, Ishii and Sadowsky 2008). It could also generate infections in wildlife of the Ayuquila, such as the neotropical river otter Lontra longicaudis. Bacterial diseases are known to affect otters elsewhere (Moore et al. 2002, Lalucat et al. 2006) and could further hinder L. longicaudis population conservation in the Ayuquila.

We carried out this study under the hypothesis that wastewaters from cities in the Autlán valley would generate an increase in the number of potentially pathogenic bacteria downstream from the areas where sewage canals empty into the river. Thus, we expected site 1 to be relatively poor in potentially pathogenic strains both in water and fish tissues. While site 1 generally had indeed a lower bacterial species richness than sites 2 and 3, pathogenic bacteria (i.e., E. coli and Pseudomonas sp.) were present throughout the river and in a high proportion of tissue samples. This was not a surprise because studies of marine microbiota in the Gulf of Mexico have also found potentially pathogenic strains even in very deep waters where there is little anthropic influence (Escobedo-Hinojosa and Pardo-López 2017). Areas upstream from site 1 in the watershed, though relatively distant (> 25 km), are also used for agriculture, free range cattle use and are sparsely inhabited (Gerritsen and van der Ploeg 2006). These could be sources for potentially pathogenic microbes in what we considered the relatively unaffected site 1.

We identified at least three species in the genus Pseudomonas. While P. fragi and P. stutzeri have no or low virulence, respectively (Lazado et al. 2015), further research is required to better identify Pseudomonas varieties in the Ayuquila. In particular, P. aeruginosa could be a potentially pathogenic strain that should be of concern for humans utilizing the Ayuquila river (Lyhs et al. 2001, Centeno and Rodríguez 2005).

Our findings provide a baseline upon which to improve our understanding of the microbiology of the Ayuquila. To surpass some of the limitations of our study, future approaches should 1) incorporate other culture media to aid in increasing the diversity of bacteria recovered from fish or water samples, 2) increase the number of samples obtained and analyzed across both, space and time, 3) use culture-independent techniques such as 16S rRNA gene taxonomic profiling methods and high-throughput sequencing to analyze water and fish samples, and 4) include as many species of fish and fauna as possible from the Ayuquila, including native species important as food or under conservation status. Improving on these limitations should allow a better understanding of the dynamics of the microbiological community in the river and provide information that could be used to prevent pathogenic bacteria in the Ayuquila river from affecting the local human population or resources in the SMBR. Further, a future study should make use of Rep-PCR molecular tools to identify the specific sources of bacteria in the watershed; other studies have found that wildlife and cattle are more pervasive sources of some bacterial species in the Ayuquila than human populations (Torres-Beristáin et al. 2013).

Subsistence freshwater fisheries in the Ayuquila and other rivers in west-central Mexico will continue to provide an important, inexpensive source of animal protein for numerous communities as long as efforts continue to abate and control pollution. Multiagency efforts have achieved many goals in controlling degradation of the Ayuquila river (Graf-Montero et al. 2006). Our results, alongside public health studies in the SMBR and urban centers in the basin, should provide guidance to reduce microbiological risks for biota and human populations dependent on the river.

ACKNOWLEDGMENTS

This manuscript results from Rosa Leonor González Díaz’s MS thesis project at the Maestría en Ciencias en Manejo de Recursos Naturales, Centro Universitario de la Costa Sur, Universidad de Guadalajara, Jalisco, Mexico. Partial support was provided by Consejo Nacional de Ciencia y Tecnología. Griselda K. Guillén-Navarro, L.V. García-Fajardo and D. Herrera-López (Laboratorio de Biotecnología Ambiental y Agroecológica (LaBTAA) at El Colegio de la Frontera Sur assisted with molecular analyses.

REFERENCES

Arellano-Ríos A. and Rivera-Pahua Y. (2011). Asociacionismo municipal y medio ambiente. La junta intermunicipal del río Ayuquila, Jalisco. Espacios Públicos 14 (3), 32-56. [ Links ]

Arvanitoyannis I.S., Stratakos A. and Mente E. (2008). Impact of irradiation on fish and seafood shelf life: a comprehensive review of applications and irradiation detection. Crit. Rev. Food Sci. Nutr. 49 (1), 68-112. DOI: 10.1080/10408390701764278 [ Links ]

Barrera-Escorcia G., Fernández-Rendón C.L., Wong-Chang I. and Ramírez-Romero P. (2013). La sensibilidad del grupo coliforme como indicador de la presencia de enterobacterias patógenas en cuatro cuerpos acuáticos de México. Hidrobiológica 23 (1), 87-96. [ Links ]

Barrett T.J., Blake T.A., Morris G.K., Puhr N.D., Bradford H.B. and Wells J.G. (1980). Use of Moore swabs for isolating Vibrio cholerae from sewage. J. Clin. Microbiol. 11 (4), 385-388. [ Links ]

Cahill M.M. (1990). Bacterial flora of fishes: A review. Microb. Ecol. 19 (1), 21-41. DOI: 10.1007/BF02015051 [ Links ]

Centeno S. and Rodríguez R. (2005). Evaluación microbiológica de pescados congelados producidos en Cumaná, estado Sucre, Venezuela. Rev. Cient-Fac. Cien. V. 15 (2), 168-175. [ Links ]

Constantino-Casas F., Armijo-Ortíz A., Osorio-Sarabia D. and Chávez-Soriano L.A. (1997). Infección por Aeromonas hydrophila e Ichthyophthirius multifiliis en trucha (Oncorhynchus mykiss, Walbaum) y tilapia (Oreochromis aureus. L) de un centro de acopio de Morelos, México. Estudio patológico. Vet. Mexico. 28 (1), 59-62. [ Links ]

Eckner K.F. (1998). Comparison of membrane filtration and multiple tube fermentation by colilert and enterolert methods for detection of waterborne coliform bacteria, Escherichia coli and Enterococcus use drinking and bathing water quality monitoring in Southern Sweden. Appl. Environ. Microbiol. 64 (8), 320-323. [ Links ]

Elías-Fernández G. and Navarrete-Salgado N.A. (1998). Crecimiento y producción de carpa común (Cyprinus carpio Linnaeus, 1758) durante época de sequía y lluvias en un bordo del Estado de México, México. Hidrobiológica 8 (2), 117-123. [ Links ]

Escobedo-Hinojosa W. and Pardo-López L. (2017). Analysis of bacterial metagenomes from the Southwestern Gulf of Mexico for pathogens detection. Pathog. Dis. 75 (5). DOI: 10.1093/femspd/ftx058 [ Links ]

García-Pérez C. and Aguilar P.A. (2013). Vigilancia epidemiológica en salud. Revista Archivo Médico de Camagüey 17 (6), 784-805. [ Links ]

Gerritsen P. and van der Ploeg J. D. (2006). Dinámica espacial y temporal de la ganadería extensiva: estudio de caso de la Sierra de Manantlán en la Costa Sur de Jalisco. Relaciones. Estudios de Historia y Sociedad XXVII (108), 165-191. [ Links ]

Graf-Montero S., Santana-Castellón E., Martínez-Rivera L. M., García Ruvalcaba S. and Llamas J.J. (2006). Collaborative governance for sustainable water resources management: the experience of the Inter-municipal Initiative for the Integrated Management of the Ayuquila River Basin, Mexico. Environ. Urban. 18 (2), 297-313. DOI: 10.1177/0956247806069602 [ Links ]

Godoy-Lozano E.E., Escobar-Zepeda A., Raggi L., Merino E., Gutiérrez-Ríos R.M., Juárez K., Segovia L., Licea-Navarro A.F., Gracia A., Sánchez-Flores A. and Pardo-López L. (2018). Bacterial diversity and the geochemical landscape in the southwestern Gulf of Mexico. Front. Microbiol. 9, 2528. DOI: 10.3389/fmicb.2018.02528 [ Links ]

Hernández-Antonio A. and Hansen A.M. (2011). Uso de plaguicidas en dos zonas agrícolas de México y evaluación de la contaminación de agua y sedimentos. Rev. Int. Contam. Ambie. 27 (2), 115-127. [ Links ]

Ishii S. and Sadowsky M.J. (2008). Escherichia coli in the environment: implications for water quality and human health. Microbes. Environ. 23 (2), 101-108. [ Links ]

Kabir S., Shahriar M., Hamidul A. N. M. and Gias M. (2006). High salt SDS-based method for the direct extraction of genomic DNA from three different gram-negative organisms. The CDR Journal 1 (2), 57-64. [ Links ]

KEGG (2017). Kyoto Encyclopedia of Genes and Genomes [en línea] Kyoto Encyclopedia of Genes and Genomes [en línea] https://www.kegg.jp 02/02/2017 [ Links ]

Lalucat J., Bennasar A., Bosch R., García-Valdés E. and Palleroni N.J. (2006). Biology of Pseudomonas stutzeri. Microbiol. Mol. Biol. Rev. 70 (2), 510-547. DOI: 10.1128/MMBR.00047-05 [ Links ]

Lazado C.C., Caipang C.M.A. and Estante E.G. (2015). Prospects of host associated microorganisms in fish and penaeids as probiotics with immunomodulatory functions. Fish. Shellfish. Immunol. 45 (1), 2-12. DOI: 10.1016/j.fsi.2015.02.023 [ Links ]

Lee Y.P., Costumbrado J., Hsu C.Y. and Yong Hoon K. (2012) Agarose gel electrophoresis for the separation of DNA fragments. J. Vis. Exp. 62, 3923. DOI: 10.3791/3923 [ Links ]

Lyhs U., Lahtinen J., Fredriksson-Ahomaa M., Hyytiä-Trees E., Elfing K. and Korkeala H. (2001). Microbiological quality and shelf-life of vacuum-packaged ‘gravad’rainbow trout stored at 3 and 8 ºC. Int. J. Food Microbiol. 70 (3), 221-230. [ Links ]

Lyons J., González-Hernández G., Soto-Galera E. and Guzmán-Arroyo M. (1998). Decline of freshwater fishes and fisheries in selected drainages of west central Mexico. Fisheries 23 (4), 10-18. DOI: 10.1577/1548-8446(1998)023<0010:DOFFAF>2.0.CO;2 [ Links ]

Mercado-Silva N., Santana Castellón E., Martínez Rivera L.M., Lyons J. and Moermond T. (2011). Subsistence fisheries in the Sierra Manantlán Biosphere Reserve (Jalisco/Colima, Mexico). e-Gnosis 9, 1-19. [ Links ]

Moore J., Heaney N., Millar B., Crowe M. and Elborn J. (2002). Incidence of Pseudomonas aeruginosa in recreational and hydrotherapy pools. Commun. Dis. Public Health. 5 (1), 23-26. [ Links ]

NCBI BLAST (2017). National Center for Biotechnology Information, Basic Local Alignment Search Tool [en línea]. http://blast.ncbi.nlm.nih.gov/Blast.cgi 02/03/2017 [ Links ]

Periago M.J., Ayala M.D., López-Albors O., Abdel I., Martínez C., García-Alcázar A., Ros G. and Gil F. (2005). Muscle cellularity and flesh quality of wild and farmed sea bass, Dicentrarchus labrax L. Aquaculture 249 (1-4), 175-188. DOI: 10.1016/j.aquaculture.2005.02.047 [ Links ]

Rincón-Rodríguez D.D., Semprún-Avendaño A.M., Dávila-Ojeda M.J., Velásquez-González H. A., Morales-Avendaño E.D. and Hernández J. (2013). Producción de harina de Spirulina máxima para ser empleada como ingrediente en la elaboración de dietas para peces. Zootecnia Trop. 31 (3), 187-192. [ Links ]

Somarelli J.A., Makarewicz J.C., Sia R. and Simon R. (2007). Wildlife identified as major source of Escherichia coli in agriculturally dominated watersheds by BOX A1R-derived genetic fingerprints. J. Environ. Manage. 82 (1), 60-65. DOI: 10.1016/j.jenvman.2005.12.013 [ Links ]

Torres-Beristáin B., González-López G., Rustrián-Portilla E. and Houbron E. (2013). Enfoque de cuenca para la identificación de fuentes de contaminación y evaluación de la calidad de un río, Veracruz, México. Rev. Int. Contam. Ambie. 29 (3), 135-146. [ Links ]

Urquía-Fernández Robles N. (2014) La seguridad alimentaria en México. Sal. Pub. Mex. 56 (supl. 1), 92-99. DOI: 10.21149/spm.v56s1.5171 [ Links ]

Received: October 01, 2018; Accepted: May 01, 2019

*Autor para correspondencia: norman.mercado@uaem.mx

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License