Marine microorganisms: the world also changes

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1 A. Marine microorganisms: the world also changes Pilar González-Párraga, Alberto Cuesta, J. Meseguer and Mª Ángeles Esteban Fish Innate Immune System Group, Department of Cell Biology and Histology, Faculty of Biology, University of Murcia, Murcia, Spain In recent years, the increasing trend of pollution has been extended to the marine environment, although it has been one of natural places more stable for years, thanks to the great development of marine aquaculture worldwide at present is being severely affected. The indiscriminate use of antimicrobial compounds begins to promote an important change in the microflora of both marine and inland waters. Microorganisms previously known as non-pathogenic or even producers of antimicrobial compounds, which had been previously described as commensally or asymptomatic organisms, begin now to be described as opportunistic pathogens, being this character often associated to stress conditions. This chapter will describe the major groups of marine microorganisms previously described as asymptomatic and members of the external bacterial microflora of fish. Within these organisms is distinguished between two groups, those who were known as asymptomatic, in which recently began to appear potentially pathogenic species or even strains and a second group consisting of bacterial type previously described as pathogenic which start having antimicrobial resistance known or permitted in the actual aquaculture practices. Keywords: Marine; drugs; resistance; bacteria. Introduction The marine environment hosts a large biodiversity and is the mainstay of economic activities with a long tradition in our society. Despite its importance as a source of food-related resources, energy or medicine, we know very little about the species of microorganisms living and functioning in aquatic ecosystems. This aquatic ecosystem includes bacteria involved in the processing of organic matter and those who live as parasites or symbionts. Many microorganisms in marine medium often produce antibacterial substances that allow the ecological stability of ecosystem [1]. These bacteria-bacteria interactions are a mechanism to keep the microhabitat to certain species of microorganisms [2]. Most of these studies have addressed the effect of other pathogenic bacteria in fish and mollusks [1]. However, these mechanisms for regulating the growth of other bacteria appear to be inhibited in situations of stress such as changes in water temperature [3]. Aquaculture is an important contribution to the nutrition of many communities around the world, but overfishing, introduction of exotic or alien species to the environment habitat or environmental degradation and water pollution have contributed to destruction and alteration of the ecosystem. One of the most serious problems facing the ocean is the pollutants from land-based sources or activities, as well as marine industrial activities such as aquaculture. The extensive freshwater or marine farming systems result in overcrowding. This increase in biomass is limited by the capacity of the marine ecosystem which brings a decline in growth, increased mortality and increased diseases. The microbiological activity is by far the most important factor influencing fish quality [4]. However, the growth and even the survival of the aquaculture industry are threatened by uncontrolled microbial diseases that cause extensive losses [5]. In this chapter we will describe some of the major bacterial species that are becoming responsible for important economic losses in the aquaculture industry in contrast to the previously well-known pathogens. Microorganisms usually described as normal in the surface microflora of fish have recently been described as opportunistic pathogens. In many cases, strains have been also described with antibiotic resistance capacity and even the inhibitory compounds produced by other bacteria of the microflora. Microorganism distribution in marine water Microorganisms are extremely important for marine life because they are essential in the destruction of organic matter. In the field of marine microbiology, the marine microbiologist CE Zobell conducted studies to demonstrate the essential role of bacteria in the cycle of living matter in seawater. In general, the higher amounts of bacteria are commonly found in the sea surface, in the highlights zone and together with the phytoplankton, and decreasing with depth. The distribution of bacteria in the seas tends to be parallel to the plankton [6]. In the sediments there are high counts of bacteria and fungi, which play an important role in the remineralization of organic matter and feeding of the deep sea fauna. Researchers believe that there are thousands of other undiscovered marine bacteria because the list of species of marine bacteria isolated to date, does not reflect the diversity of forms present in the sea. Some of these marine bacteria present great difficulties in identification or taxonomy because of its difficult isolation and culture since many of them have special needs for growth or are only able to grow associated with other organisms [3]. There are not marine FORMATEX

2 common the presence of plasmids and do not form spores. Some species synthesize an exopolysaccharide capsule that facilitates cell adhesion, biofilm formation and protects against phagocytosis, antibody or complement binding, thus increasing its pathogenicity [40]. Pseudomonas are characterized by an enormous metabolic capacity which is reflected by their capability to adapt to diverse environments, such as terrestrial and marine, degrade compounds and synthesize great variety of molecules. Pseudomonas is the most common genera in crustaceans, marine fish and bivalves [41]. A major factor in its prominence as a pathogen is its intrinsic resistance to antibiotics and disinfectants [42]. Plasmids and bacteriophages are important contributors to the genetic diversity found in Pseudomonas sp [42]. Pseudomonas aeruginosa participates in infections in immunocompromised patiens and has emerged as a model organism for biofilm studies. The group of bacteria related to the genus Pseudomonas is very broad and includes species pathogenic for humans and plants commonly found in fresh altered water. In the case of marine organisms species of the genus Pseudomonas have been isolated and identified from the microbiota of farmed fish such as rainbow trout (Oncorhynchus mykiss) [43], perch (Perca fluviatilis) [44] and rohu (Labeo rohita) [45]. There are also data that report the role as a fish pathogen of some species such as P. fluorescens [46], P. anguilliseptica, which has been identified as the cause of mortalities in Japanese eel (Anguilla japonica) and European eel (Anguilla anguilla), gilthead seabream (Sparus aurata) and turbot (Scophthalmus maximus) [47, 48, 49]. P. plecoglossicida causes hemorrhagic ascites in freshwater fishes of Japan [50] and P. luteola causes mortalities in rainbow trout [51, 52] and there are other diseases in fish that have not been determined the Pseudomonas species that has caused them [53]. Korkea-Aho et al [54] have described that Pseudomonas M174 strain is a potential probiotic against Flavobacterium psychrophilum and has several modes of action. An additional property of Pseudomonas sp is their resistance to many antibiotics [55]. Pseudomonas aeruginosa is responsible for a high percentage of nosocomial infections. The difficulty in its treatment by antibiotics arises from its capability of nearly expressing all mechanisms of antibiotic resistance; hence, it is considered a multidrug-resistant (MDR) organism [56]. Many compounds have been identified as efflux pump inhibitors (EPIs) when used as adjuvants or in combination with the effective antibiotics [56]. Certain parameters are essential for choosing between the general EPI that can inhibit the action of one transporter that expels various antibiotics in one bacterial species or a specific EPI that inhibits the pumping of one antibiotic family in various bacteria [56]. Genus Psychrobacter Psychrobacter are psychrophilic and halophilic microorganisms, aerobic, stationary and catalase and oxidase positive, also show no pigment [57]. The optimum growth temperature is about 20º C but authors have described Psychrobacter strains which can growth about -10º C until 26º C [58]. The Psychrobacter strains have diverse representatives of the permafrost community, should carry traits that has allowed them to adapt to these conditions [58]. Changes in membrane composition and exopolysaccharides are the results of growing in presence and absence of 5% NaCl [58]. The role of the genus Psychrobacter as a pathogen is unclear and reported only one species, Psychrobacter immobilis, which was isolated from rainbow trout showing a natural infection [59]. Under certain experimental conditions, infection with Psychrobacter immobilis failed to produce mortalities although external symptoms, such as darkening of the skin, pale gills and abnormal swimming and other internal symptoms such as dilation of vascular structures, infiltration of mononuclear cells in the liver, degeneration of gills, vascular congestion, etc. were described [59]. The microorganism P. marincola is described as new specie of the genus Psychrobacter by Romanenko et al [57], which was isolated from seawater samples as well as tissues of a tunicate. Resistance to antibiotics of Psychobacter is beginning to be described. Some authors have described that this sensitivity or resistance depends on the particular strain and the growth temperature [58]. Sulfonamide resistance was reported for the first time by Byrne-Bailey et al [60] and a Psychrobacter psychrophilus strain has been described like resistant to tetracycline and streptomycin was isolated from subsoil sediment sampled from the coast of the Eastern- Siberian Sea. The genes conferring antibiotic resistance were localized on a plasmid [61]. Genus Alteromonas Alteromonas is a genus of gram-negative aquatic bacterium with curved rods and motile by means of a single polar flagellum; require a seawater base for growth. Alteromonadaceae family includes genera such as Alteromonas, Pseudoalteromonas, Marinobacter and Shewanella which include marine bacteria. Encompassed many of the bacteria in the genus Alteromonas previously have been relocated to the genus Pseudoalteromonas after phylogenetic analysis of 16S rrna, as in the case of Alteromonas elyakovii [62] is currently identified as Pseudoalteromonas elyakovii. Pseudoalteromonas genus has species associated with marine organisms, but only some of them are related to disease. This is the case of certain crustaceans and mollusks [63]. In an epidemiological study, representatives of four species of Pseudoalteromonas were isolated from the internal organs of European sea bass (Dicentrarchus labrax) and seabream [64]. In addition, this genus proved to be the prevalent microorganisms isolated from sea bass showing clinical symptoms and gold without it. However, in experiments to test the possible pathogenicity of these species could be demonstrated that only one of the species tested, identified as P. undine, was weakly virulent to sea bass FORMATEX 2011

3 some ECPs that are closely related to its virulence [93]. The pathogenicity of this species to induce disease in certain fish, such as rainbow trout [94] has also been reported and their description among the dominant members of the intestinal microbiota of larval seabream and sea bass [95]. Some Vibrio species isolated from Italian aquaculture showed resistance to ampicillin, carbenicillin, kanamycin, cefalothin, while they were sensitive to chloramphenicol, nitrofurantoin and tobramycin; the sulfadiazine-trimethoprim association was completely ineffective [96]. The treated effluent systems are reservoirs for various antibiotic resistance genes and Vibrio species isolated from wastewater final effluents showed resistances against erythromycin (100%), chloramphenicol (100%), nitrofurantoin, cefuroxime and cephalothin (90-95%) [97]. Genus Photobacterium Microorganisms included in the genus Photobacterium are gram-negative rod-shaped bacteria, halophilic, facultatively anaerobic, that are common in the marine environment and on the surfaces and in the intestinal contents of marine animals. Some species are bioluminescent and are found as symbionts in specialized luminous organs of fish. P. phosphoreum contains in its genome a lux gene that codes for the enzyme luciferase. This enzyme transforms chemical energy into light energy. Luciferase is a heterodimer with alpha and beta subunits. These two subunits are coded by luxa and luxb respectively [98]. Photobacterium includes species that are pathogenic for various farmed fish. P. damselae subsp piscicida [99] previously named Pasteurella piscicida, which has been described as the aetiological agent of pasteurellosis in marine fish. Adherence by a polysaccharide capsule and extracellular products are an important first step in the pathogenesis of this disease, P. damselae subsp damselae [100] and species that have a symbiotic relationship with fish [101]. Other members of this genus have been described as members of the intestinal microbiota of Nephrops norvegicus [102], Salmo salar [103] and certain corals [104]. Photobacterium damsela subsp piscicida isolated from different geographical areas, found that the majority (93%) of the isolates were resistant to erythromycin, and also, in a lower percentage (less than 10%), to amoxicillin, ampicillin, florfenicol and trimethoprim-sulfamethoxazole [96]. In particular, European P. piscicida isolates were sensitive to kanamycin, florfenicol and trimethoprim- sulfamethoxazole while the Japanese strains are more resistant [96]. Genus Aeromonas The genus Aeromonas comprises gram negative rod, facultative anaerobic, non-sporulating, motile with a single polar flagellum and grow in the temperature range of mesophilic [40]. Individuals are ubiquitous in fresh and salt water. The genus Aeromonas belongs to the Vibrionaceae family, and has many similarities to the family Enterobacteriaceae. The genus is divided into two groups: the group of psychrophilic Aeromonas which consists of a single species, A. salmonicida and mesophilic Aeromonas group is formed by the species A. hydrophila, A. caviae, A. veronii subsp. sober, A. jandaei and A. veronii subsp. schubertii. Aeromonas hydrophila behaves as an opportunistic pathogen in both aquatic and host environments. It can cause hemorrhagic septicemia, resulting in fin and tail rot and epizootic ulcerative syndrome in juvenile and mature fish or intestinal and wound infection in human [105]. Usually, the identified species of this genus such as Aeromonas bivalvium, Aeromonas hydrophila and Aeromonas salmonicida subsp. salmonicida are associated with marine organisms. The first one was firstly described as a new species of the genus Aeromonas by Minana-Galbis et al [106], following the identification of a strain isolated from bivalve mollusks. However, it has not been described as fish pathogens so far. Aeromonas hydrophila is a ubiquitous organism found in the microbiota of different fish and other aquatic organisms. It can cause disease under stress conditions and is the causative agent of the disease known as hemorrhagic septicemia, or ulcerative disease [107]. This is a microorganism implicated in several epizootic outbreaks in aquaculture [108], some of them affecting sea bass [109]. Fish infected with this bacterium have different symptoms that can range from a lack of appetite, abnormal swimming, pale gills and skin ulcerations [110]. In Atlantic salmon, A. salmonicida causes the disease known as furunculosis and it causes lesions in the dermis, leading to ulcers, added to its ability to penetrate the tissues and organs [20]. It has been isolated from various fish such as salmon, perch, carp, different types flounder, eel, catfish, etc. [111], but has virtually no impact on the golden crops and there is a reference to an infection by A. salmonicida achromogenes in sea bass in Turkey [112]. In particular, Aeromonas is one of the major causes of bacterial infections affecting tilapia [113]. The pathogenicity of A. hydrophila depends on the production of potential virulence factors, such as exoproteases and exotoxin [105]. Application of antibiotics and chemical drugs is a conventional method to control this disease, but generally results in the constant emergence of "superbugs" and chemical accumulation in the food chain [105]. Pathogenic strains of Aeromonas veronii resistant to multiple antibiotics were isolated from A. ocellatus individuals showing signs of infectious abdominal dropsy. The moribund fish showed haemorrhage in all internal organs, and pure cultures could be obtained from the abdominal fluid [114] FORMATEX 2011

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