Predominant bacterial pathogens causing disease of
1. Introduction
Global shortages in seafood resources have driven the growth of aquaculture as an economic activity, predominantly in developing countries [1-2]. As a consequence of space and resource constraints, traditional aquaculture has been intensified into reticulated systems with high stocking densities of the cultured species [3-4]. This results in an artificial environment that has a propensity for supporting the growth of pathogenic bacteria and the accumulation of waste metabolites in aquaculture systems [5]. The indiscriminate release of spent aquaculture wastes into surrounding environments is also problematic [6-7].
The outbreak of disease in aquaculture systems, caused by bacterial pathogens, is a complex phenomenon associated with stressful environmental conditions such as poor water quality and can ultimately result in mass mortality and significant loss to the industry [8-9]. The main cause of poor water quality is waste accumulation through hyper-nutrification resulting from excessive feeding rates and high nutrient dietary composition, both of which are common phenomena in intensive aquaculture systems [13-15]. High levels of nitrogenous and phosphorous waste accumulation predispose fish to infestation by parasites and pathogens and also pose a threat to the environment [13,16-17]. Selection for certain characteristics by breeders has also in some cases reduced the vigour in breeding lines, making fish less hardy and more susceptible to disease [10]. Of particular importance is the prevalence of bacterial disease, which results in damage and often leads to death of fish [11]. Gram-negative bacteria such as
Useful micro-organisms play a number of roles in pond culture, particularly with respect to productivity, nutrient cycling, nutrition of the cultured animals, water quality, disease control and environmental impact of effluents [22-24]. Bacterial additives demonstrate the potential to improve water quality and reduce pathogen load and mortality, and have thus emerged in modern day aquaculture as alternatives to chemicals and antibiotics [17,24]. Many bacterial strains have also demonstrated a significant algaecidal effect, which is advantageous in aquaculture systems through reduction of algal growth and hence algal blooms which can destabilise these systems [25-26]. Biological agents such as Gram-positive
2. Aquaculture as an economic activity
The Food and Agriculture Organization of the United Nations [28] reported that capture fisheries and aquaculture supplied the world with about 154 million tonnes of fish in 2011, of which 131 million tonnes were used for human consumption [28]. Aquaculture contributed 79 million tonnes to the global fisheries market in 2010 at a value of $125 billion. Aquaculture farming used for food consumption comprised 60 million tonnes ($119 billion), 15 million tonnes was used for fish meal and fish oil production, while the remainder was used for ornamental fish production. With sustained growth in fish production and improved distribution channels, world supply of fish for human consumption has grown dramatically in the last five decades. An average growth rate of 3.2% per year in the period 1961–2009, has outpaced the increase of 1.7% per year in the world’s population. The global aquaculture market comprises both marine and inland (freshwater) farming. The majority (90%) of fresh water ornamental fish are captive bred, compared to only 25 of the 8000 species of marine fish. In 2010, 75% of the quantity of fish and fishery products produced consisted of products destined for human consumption, with ornamental aquaculture contributing a smaller volume.
Aquaculture production is dominated by developing countries, and predominates in Asian countries. The methods of practice of aquaculture have evolved into intensive reticulated systems, in contrast to traditional extensive systems, due to restrictions in availability of land and as a consequence of increased environmental awareness. Aquaculture is probably the fastest growing food-producing sector globally, and the most recent estimates for worldwide aquaculture show that it contributes just over 50% of total fish production. This has been an astonishingly fast growth rate from only 16% of total consumption 15 years ago. The key impetus for growth of the market is global food security and a resistance towards resource exploitation through over-harvesting of natural waters [29]. The consumer drives the aquaculture practice, product quality and branding. End products must thus address consumer food concerns and must at least be as desirable as naturally harvested products.
3. Current challenges of the aquaculture industry
Key challenges to the development and growth of aquaculture as an economic activity are limited water resources, energy requirements and the environmental impact of aqua-farming methods. To address these challenges water is re-cycled and farming activities are intensified, resulting in an increase in stocking density, deterioration in water quality, increased incidence of disease, poor feed to body mass conversion efficiencies and higher mortality rates. The net result is reduced yield. Annual losses to the market due to disease, water quality and nutrition are estimated at 40% [30].
3.1. Disease in aquaculture
Definitions of disease include an unhealthy condition or infection with a pathogen. Disease is a complex phenomenon, leading to some form of measurable damage to the host [12]. Outbreaks of disease either begin suddenly and progress rapidly, often with high mortalities, and disappear with equal rapidity (acute disease) or develop more slowly with less severity, but persist for greater periods (chronic disease). Fish disease is the outcome of aberrations to the delicate interaction between the hosts, the disease-causing agent, and external conditions such as unsuitable changes in the environment, poor hygiene and overcrowding. Disease outbreak is generally associated with a primary invasion by parasites or mechanical injury, coupled to stressful environmental conditions such as changing temperature and poor water quality [8]. The prevalence of infectious agents can result in mass mortality causing significant losses to aquaculture operations [9]. Fish diseases such as rotting fins and ulceration of the skin are more prevalent when fluctuation in temperature causes immuno-modulation, resulting in inferior disease resistance and increased mortality [31-32]. An array of stress factors such as poor water quality, parasite load or a natural physiological state (e.g. during the reproductive phase) in the life cycle of the fish are also often associated with outbreaks of disease [12]. Strict selection for desirable characteristics by breeders has also reduced the vigour in breeding lines, making fish less hardy and more susceptible to disease [35]. Disease is not necessarily caused by the action of a single bacterial taxon, as representatives of many bacterial taxa have at one time or another been associated with disease outbreaks.
Environmental factors play a key role in the onset of disease which is reported as being a consequence of the interaction between the host, environmental stress and prevalence of disease causing agents [8,12,34]. Some diseases are prevalent in spring and associated with environmental change to warmer temperatures, a period which is also characterised by an increase in the activity of pathogenic bacteria and parasites. Temperature fluctuation causes transient immuno-modulation of fish, which can result in reduced disease resistance [31-32]. Haemorrhagic septicaemia is an example of this phenomenon, with the disease resulting from infection by a wide range of pathogens that cause open ulcerated lesions and haemorrhages on the infected fish [12,36-37]. Additional clinical symptoms can include fin and tail rot, the loss of scales, localized haemorrhages, particularly in the gills and vent, exophthalmia and abdominal distension [12]. The acute form of this disease is of sudden onset, and the fish usually die within 2-3 days [38-40]. The main pathogenic micro-organisms involved in septicaemia are
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Haemorrhagic septicaemia, motile |
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Furunculosis, carp erythrodermatitis, ulcer disease. |
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Generalized septicaemia |
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Skin ulceration |
3.2. Water quality
Use of reticulated systems for intensive culture results in substantial amounts of particulate organic and soluble inorganic excretory waste, due mainly to increased stocking density [17]. The main source of this waste is hyper-nutrification, resulting from excessive feeding rates and high nutrient dietary composition, which has a significant influence on the survival, growth and reproduction of fish [13-15,17,46]. Nitrogen and phosphorous waste accumulation pose a threat to the environment and can predispose fish to infestation by parasites and pathogens due to a reduction in immunity [13,17].
Ammonia is a primary metabolic waste of fish and is excreted through the gills by bronchial diffusion. It is also produced by bacterial ammoniafication of uneaten food and faeces and is released from the mineralization of sediment [47-50]. Ammonia is oxidised to nitrite and finally to nitrate through the process of nitrification, with ammonia and nitrite being the most toxic of these metabolites to fish. Nitrite can also be produced through the process of denitrification [48]. Ammonia concentrations above 0.3 mg/l have been reported as toxic to fish, with hyperplasia of gill tissue, gill necrosis, pathological evidence of kidney and liver damage and reduction in growth rate occurring at this and higher concentrations [51-53]. Exposure to high ammonia concentration also causes epithelial lifting on gill filaments resulting in respiratory impairment and mortality [54]. Nitrite is usually present at low concentrations in natural systems, except when there is an imbalance, because it is a common intermediate in nitrification and denitrification, catabolic ammoniafication and nitrate assimilation [55]. Through denitrification, nitrite can be produced as an intermediate in the conversion of nitrate to nitric oxide, nitrous oxide and nitrogen gas [56]. Nitrite is considered harmful to fish at levels of 0.15 mg/l and above, causing conversion of haemoglobin to methaemoglobin in blood, which results in inhibition of oxygen transport and mortality due to brown blood disease [13]. Increased concentrations of nitrite also significantly affect weight gain, specific growth rate and food conversion efficiency [57].
Dietary phosphorous is an essential component of fish feeds as it improves weight gain and feed conversion ratio. It is however poorly utilized due to the absence of an acidic stomach in some species and because phosphate is often bound to phytic acid in vegetable protein [58]. Ingested phosphorous is therefore lost in faeces and results in poor water quality with increased algal growth and eutrophication [59-60].
4. Conventional approaches for addressing challenges in aquaculture
The rearing of fish in reticulated systems results in a highly artificial environment which has a propensity for the accumulation of waste metabolites and which promotes the growth of pathogenic bacteria. Management considerations for aquaculture operations include nutrition, water quality, physical parameters and pathogen and disease control [61]. Chemicals are often used to control disease and include a wide range of topical disinfectants, organophosphates, antimicrobials and parasiticides to deal with disease and water quality [18,26]. Water quality is traditionally managed through conventional reticulated filtration systems, which are sensitive to process fluctuations and can result in mass mortality when the systems crash.
4.1. Use of chemicals in aquaculture
Antimicrobial agents are extensively used for treatment during disease outbreak or at prophylactic doses to prevent outbreak of disease. This can lead to antibiotic resistance and increased virulence of pathogenic organisms, leading to a requirement for high doses of existing drugs or new drugs to control disease [5,17,20]. Antibiotic resistance can pose a risk to human health and can cause mass mortality of fish [63]. Studies have also demonstrated that chemicals used in aquaculture can be toxic to the fish themselves, with exposure to some chemicals causing a stress response and blood biochemical changes [17,21,64]. The presence of higher drug concentrations, and an ever increasing spectrum of chemical residues, can result in detrimental effects to consumers and the environment [62]. These chemicals also have a negative impact on the aquaculture filtration systems themselves, resulting in a deterioration in water quality. Chemicals are often recalcitrant, persisting for several days to months, and can cause alterations in naturally occurring bacterial populations, Regulators have recognised the risks posed by use of chemicals as substantiated by the ever increasing list of banned substances, a consequence of which is a reduction in treatment options for aquaculture [24,65-66]. Governments and organizations have recently introduced much tighter restrictions on the use of antibiotics in animal production. As an example, the European Union (EU) banned the use of avoparcin in 1997 and in 1999 included virginiamycin, spiramycin, tylosin and bacitracin as banned growth promoters in animal feeds [67-68].
4.2. Conventional biofiltration
Normally the oxidation of ammonia to the more benign nitrate ion occurs through ammonia and nitrite oxidising obligate chemoautotrophs such as
5. Biological solutions as alternatives for addressing challenges in aquaculture
Given the challenges in conventional aquaculture practise, alternative methods for disease control and enhancement of water quality are desperately required. Micro-organisms play important roles in aquaculture, particularly with respect to nutrient cycling and the nutrition of the cultured animals, water quality, disease control and the environmental impact of effluent [22]. Beneficial microbes can be used to alter or regulate the composition of bacterial flora in a water system to optimise fish production by reducing pathogen concentration, by improving water quality through reduction of waste ions and through accelerated mineralization and nitrification, by reducing algal growth and by accelerating sediment decomposition [17,20,70-71]. These biological agents also confer the added advantage of natural integration into existing ecosystems and present opportunities for development of multi-effect products which are attractive to end users. The marketing of biological and “organic certified” solutions for enhancement of fish health has also gained consumer acceptance. The use of beneficial microbes is a more appropriate remedy than the use of chemicals but successful application requires an understanding of the ecological processes occurring in aquaculture systems, of the agents responsible for disease and knowledge of the beneficial characteristics of bacteria to be used as biological agents [5,72].
5.1. Biological agents
Microbial webs are an integral part of all aquaculture systems and have a direct impact on productivity, especially in intensive culture operations. The quality of water and health of the cultured species is governed by the activities of a diversity of microbes with different roles and interactions in the ecosystem [61]. There are distinct uses of bacterial supplements in aquaculture for bio-augmentation as probiotics and as biocontrol and bioremediation agents [19]. Bio-augmentation refers to the augmentation of the environment and/or the microbes to result in enhanced fish health while probiotics are normally associated with feed and digestion. A strict definition of biocontrol agents are microorganisms that are antagonistic to pathogens. In some instances however the description of biocontrol agents transcends the boundary between bio-augmentation, and the exclusion of pathogens [73]. Bioremediation refers to the breakdown of pollutants or waste by microbes [5,61].
A probiotic can be defined as a cultured product or live microbial feed supplement which beneficially affects the host by improving its intestinal balance [74]. The important components of this definition reflect the need for a living microorganism and application to the host as a feed supplement. A broader definition is that of a live microbial supplement, which beneficially affects the host animal by improving its microbial balance [75]. In a third proposed definition, a probiotic is any microbial preparation, or the components of microbial cells, with a beneficial effect on the health of the host [76]. It is thus apparent that there are variations in the actual application of the terminology associated with biological agents [77]. Based on the observation that organisms are capable of temporarily modifying the bacterial composition of water and sediment, it was suggested that the definition should include the addition of live naturally occurring bacteria to tanks and ponds [73]. Verschuere
The range of biological treatments examined for use in aquaculture has encompassed both Gram-negative and Gram-positive bacteria, bacteriophages, yeasts, unicellular algae, enzyme preparations and plant extracts. Microbes have been successfully applied to aquaculture systems via inclusion in artificial or live feed, by addition to biofiltration systems and by direct addition to water [77]. Most biological treatments used in aquaculture belong to the genera
5.2. Modes of action of biological agents
Mechanisms of probiosis include competition with pathogens for adhesion sites, immune stimulation, synthesis of antimicrobials, competitive exclusion, bioaugmentation and bioremediation [23-24,26,78]. Although many biological treatments have been developed over the last decade, the approach used has generally been empirical and the exact modes of action were rarely elucidated, negatively affecting technology adoption and implementation in aquaculture [26].
One possible mechanism for preventing colonization by pathogens is competition for adhesion sites on gut or other tissue surfaces [78]. It is known that the ability to adhere to enteric mucus and cell wall surfaces is necessary for bacteria to become established in fish intestines [79-80]. The ability to adhere and grow on or in intestinal or external mucus has been demonstrated for fish pathogens in
Immuno-stimulants are chemical compounds that activate the immune system of animals and render them more resistant to infections [84]. Fish larvae, shrimps, and other invertebrates have immune systems that are less well developed than their adult counterparts and are dependent primarily on non-specific immune responses for their resistance to infection [85]. Bacteria may act as immuno-stimulants in fish and shrimp, but it has not yet been conclusively demonstrated that they have a beneficial effect on the immune response of cultured aquatic species [26,86].
Microbial populations may release chemical substances that have a bacteriocidal or bacteriostatic effect on other microbial populations, which can alter inter-population relationships. The presence of bacteria producing inhibitory substances is thought to constitute a barrier against the proliferation of opportunistic pathogens. In general, the antibacterial effect of bacteria is due to the production of antibiotics, bacteriocins, siderophores, enzymes, hydrogen peroxide or alteration of pH by the production of organic acids, ammonia or diacetyl [26]. Many authors assign the inhibitory effects detected in
Competition for nutrients or available energy may determine how different microbial populations coexist in the same ecosystem, but to date there have been no comprehensive studies on this subject [87]. Competitive exclusion is an ecological process that allows manipulation of the bacterial species composition in water, sediment or the host itself, by competitive assimilation of nutrients and/or an intrinsically higher growth rate [5,23-24]. The microbial ecosystem in aquaculture environments is generally dominated by heterotrophs competing for organic substrates as both carbon and energy sources. Competitive utilization of these substrates can thus attenuate target pathogenic microorganisms as demonstrated by several studies. A bacterial strain selected for its active growth in organic-poor medium, was reported to prevent the establishment of a
Virtually all microorganisms require iron for growth [88]. Siderophores are low molecular weight (< 1,500), ferric ion-specific chelating agents that can dissolve precipitated iron thus making it available for microbial growth [89]. The ecological significance of siderophores resides in their capacity to scavenge an essential nutrient from the environment and deprive competitors from accessing it. The requirement for iron is high for many pathogens in highly iron limited environments [88,90] and several studies have reported a correlation between iron availability and pathogen growth. In a challenge test with pathogenic
Improvement in water quality has been recorded in studies involving the addition of biological agents. These improvements include the reduction of total and dissolved solids concentrations, lower concentrations of waste ions and a reduction in algal populations. Gram-positive bacteria are generally more efficient in converting organic matter to CO2 than Gram-negative bacteria, which convert a greater percentage of organic carbon to bacterial biomass or slime. By maintaining higher levels of these Gram-positive bacteria in production systems, farmers can reduce the build-up of dissolved and particulate organic carbon during the culture cycle [26]. Nitrite accumulation may be caused by imbalances in the activities of nitrate and nitrite reductase and inhibition of nitrite reductase by oxygen. Bio-communities however usually contain bacteria with different nitrate and nitrite reductase activities enhancing the denitrification efficiency of the overall bio-community [93]. Although the specific nitrification activity of heterotrophic bacteria is generally lower than that of chemoautotrophs, the overall impact on denitrification could be greater due to the higher cell numbers of heterotrophic bacteria and their robustness to process fluctuations. There is therefore merit in utilizing biological agents for nitrification and phosphate bioremediation to improve water quality in aquaculture [26,86]. Many bacterial strains have been shown to have a significant algaecidal effect on various species of micro algae [26,94-95]. This effect is valuable where algal blooms may be problematic, causing blockages to flow systems and changes in oxygen concentration due to algal cellular respiration.
Formulation of bacterial consortia with interactive effects, including pathogen inhibition, high growth rate and improvement in water quality, provides broad spectrum effects in a single product [72]. Lalloo
5.3. Bacillus spp . as attractive biological agents
The application of
Several studies have demonstrated the application of
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Premixed with feed | [105] |
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Added to water | [106] |
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Penaeids | In water | [61] |
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Channel catfish | In water | [96] |
Mixed culture, mostly |
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Mixed with water | [107] |
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In water | [72] |
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Turbot larvae | In water | [19] |
6. Isolation, screening and selection of candidate biological treatment agents
There is an elegant logic in isolating putative biological agents from the host or the environment in which the agents are likely to exert a beneficial effect, but there is no unequivocal indication that these isolates perform better than isolates completely alien to the cultured species or originating from a different habitat [26]. A combination of methods and incubation conditions need to be used to achieve pure cultures of target organisms. To an extent, the range of media to be used is governed by personal choice and experience [12]. Many bacteria that are residents of soil and aquatic habitats low in nutrients have difficulty growing in rich media. Also, many potential contaminants cannot compete in dilute media, so the limitation in nutrient availability becomes a selective factor. In order to appropriately select biological agents it is essential to understand the mechanisms of action and to define selection criteria for potential microbes. A classical screening and selection rationale may include collection of background information, acquisition of isolates, purification of isolates and evaluation based on pre-determined criteria for both
6.1. Isolation of biological agents
When selecting desirable biological agents enrichment techniques that make it possible to exploit the differential characteristics of target isolates in mixed microbial populations should be applied.
6.2. In vitro screening and selection of aquaculture biological agents
To appropriately select biological agents it is essential to understand the mechanisms of action and to define selection criteria for potential probiotics [112]. Many bacteria have been exploited as biological agents but their selection has been based mainly on empirical observations rather than scientific data [71].
A common protocol for screening candidate biological agents is to perform
In aquaculture, bioremediation or bioaugmentation is an important selection criterion, particularly under conditions that mimic the application environment [5]. While some studies have reported screening strategies to select for the bioremediation capabilities of potential aquaculture biological agents, this area has regrettably not been well reported to date [27,72]. Recent studies by Lalloo
Once candidate biological agents are selected, proper identification and safety assessment is an important requirement prior to application
6.3. In vivo validation of the efficacy of putative biological agents
Once candidate biological agents have been selected, the next important step is confirmation of observed efficacy using
6.4. Other considerations during selection of biological agents
Strains showing well-established biological effects in
7. Bio-production of biological agents
Large scale production of probiotics is an essential step towards application in the aquaculture industry as production cost is an important consideration in the development of commercially relevant biological products [126]. The cultivation of microorganisms at a large scale is influenced by various factors such as the composition of the media, as well as physical and chemical variables [127]. It has been widely documented that nutrient sources influence the growth, spore production, and synthesis of commercially useful metabolites in
7.1. High cell density cultivation of Bacillus spp .
Although
The type of carbon source and the carbon to nitrogen ratio play an important role in microbial growth [142]. It has been observed that
Various protein substrates have been tested for the growth and synthesis of commercially useful metabolites by
7.2. Production of spores
The key challenge in spore production is to maximize sporulation from a high density vegetative cell culture [134,139]. Environmental signals for sporulation include culture density dependant peptides, oxygen availability and limitation of carbon, nitrogen or phosphorous [140]. The life-cycle of a spore forming bacteria consists of four stages i.e. vegetative growth, sporulation, germination and outgrowth [139,159]. Cells enter a sporulation pathway, which involves three differentiating cell types, namely the predivisional cell, mother cell and the forespore, in response to nutrient limitation [160]. The forespore undergoes dehydration, while the cortex is produced between the two membranes that separate the mother cell and the forespore. Eventually the mature spore is released when the mother cell lyses. This mature spore has the ability to remain dormant for long periods of time [160]. The most important sporulation related transcriptional regulator is Spo0A which is phosphorylated via a complex network of interactions in response to nutrient limitation [140,161]. Furthermore, genes in the Res system are induced under anaerobic growth conditions which contribute to the sporulation cascade during oxygen insufficiency [162]. Low phosphate concentration results in the earlier onset of sporulation due to the response of the Pho system to phosphate starvation [162]. Magnesium sulphate, calcium carbonate and phosphate all stimulate sporulation, whereas divalent cations (particularly Ca2+) assist in dehydration and mineralization of the spore [154,161]. According to Monteiro
8. Application of biological agents
A key challenge for usefulness of biological agents is the survival of the micro-organisms in the environment to which they are applied. Biological agents must thus be tolerant to the prevailing environmental conditions in which they are expected to perform, often dictated by the species being cultured for a specific aquaculture application [49]. Several methods of addition of biological agents to the host or its ambient environment exist, with each application method presenting unique challenges to the survival and efficacy of the biological agent [26,71,118,165]. A biological agent must provide actual benefit to the host, be able to survive in the environment of the intended application and should be stable and viable for prolonged storage and in the field [77]. Other factors such as natural deterioration and washout of the biological agent may necessitate the on-going addition of the treatments to maintain their positive effect [26]. Information on the robustness and functionality of biological agents in response to environmental conditions such as salinity, pH and temperature are however limited. Lalloo
For the application of spores as aquaculture biological agents, determination of their functionality as antagonists to disease or for improvement in water quality under the physiological ranges to be encountered in the aquaculture system is thus an important requisite [88]. Changes in growth conditions such as temperature constitute a key factor that influences cell growth and survival of
9. Future prospects of the technology
The traditional practise of extensive land based aquaculture is under pressure, due to a limitation in available space, which has led to the increased use of more intensive reticulated systems which also offer the benefit of greater control of physiological culture conditions. While intensive systems offer the advantages of increased stocking densities and higher production throughput, challenges include water quality and increased disease prevalence among others. These are driving the adoption of environmentally friendly solutions that meet consumer expectations and comply with regulatory requirements. Biological solutions provide an attractive option. Issues that require attention to accelerate the adoption of biological solutions include the elucidation of the mode of action of commercial biological products and demonstration of clear cost-benefit advantages for commercial products.
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