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A Fishy Business The pathogenicity and control of pathogens bedeviling aquaculture are becoming increasingly urgent research agendas for fish microbiologists Bernard Dixon I think I have detected an increase in the frequency of papers appearing in wide-ranging microbiology journals on fish infections and methods of combating them. If reports on piscine pathogens are indeed spilling over from their appropriate specialized publications into the general literature, there is a highly plausible clutch of linked explanations. Firstly, the traditional toil of hauling fish out of the seas in nets has, like cattle ranching on land, reached its productive limit. Secondly, this shift has triggered a massive expansion of fish farming, which is now the fastest-growing sector of the world’s food economy. Having risen by an average of 11% per year over the past decade, aquaculture is expected to overtake beef production as a source of food by 2010. Thirdly, these seismic changes are underlining the pressing need to deal more effectively with the largest causes of financial losses in aquaculture: the moulds and bacteria responsible for fish diseases. Saprolegnia, an oomycete (water mould) related to the Phytophthora infestans which precipitated the Irish potato famine at the end of the 19th century, is attracting particular concern. As pointed out by Pieter van West of Aberdeen University in Scotland, the dangers posed by this ever-present threat to fish farms have been exacerbated by a decision six years ago to prohibit the agent formerly deployed against the organism. “Up until 2002, Saprolegnia infections in aquaculture were kept under control with malachite green, an organic dye that is very efficient in killing the pathogen,” van West writes in Mycologist (20:99 –104, 2006). “However, the use of malachite green has been banned worldwide due to its carcinogenic and toxicological effects. . . This has resulted in a dramatic reemergence of Saprolegnia infections in aquaculture. As a consequence Saprolegnia parasitica 108 Y Microbe / Volume 3, Number 3, 2008 is now, economically, a very important fish pathogen, especially on catfish, salmon and trout species.” Enthusiasts with fish tanks at home are familiar with Saprolegnia as an occasional nuisance in the form of white or grey patches of filamentous mycelium on the body or fins of freshwater species. On a world scale, however, it is a formidable foe. As van West emphasizes, it has not only contributed to crashes in natural populations of salmonids throughout the world. It also causes losses of millions of dollars annually for the aquaculture businesses of the United States, Canada, Scotland, Scandinavia, Chile, and Japan. In the absence of malachite green, the few alternative chemicals that do staunch the disease in salmonid eggs do not give adequate protection after hatching. Hopes are now pinned on future advances in understanding the basic molecular processes of this ferocious water mould, its interactions with susceptible fish, and the identification of the relevant genes and proteins. It’s possible, perhaps likely, that such developments will spawn new strategies to help the ailing aquaculture industry. Meanwhile, one recent development is already being harnessed in the battle against bacterial fish diseases. This is the use of naturally antagonistic organisms, thought to function either by competitive inhibition, by nonspecifically enhancing immunity, or by modifying the environment. Categorized as probiotics (and associated with a similar mixture of genuine science and hocus-pocus as that which surrounds probiotics in humans), they are already being incorporated into fish feed. While some of these organisms are lactic acid bacteria, other genera and species are showing a greater degree of genuine efficacy. One recent example is the Bacillus subtilis AB1 which Brian Austin and coworkers at Heriot-Watt University, Edinburgh, and the University of West Indies in St. Augustine, Trinidad, have developed as a putative agent to combat species of Aeromonas which attack rainbow trout. As described in the Journal of Applied Microbiology (103:1699 –1706, 2007), the organism was one of several obtained from the digestive tract of euthanized rainbow trout and selected for its inhibitory activity against a pathogenic aeromonad recovered from diseased tilapia. When healthy rainbow trout received the B. subtilis AB1 in their feed for 14 days, they survived challenge with the pathogen. In immunological assays, the bacillus also specifically stimulated respiratory burst, serum and gut peroxidase activities, phagocytic killing, total and alpha-1 antiprotease activities, and lymphocyte populations. “The fact that B. subtilis AB1 was isolated from the gut of apparently healthy rainbow trout confirms the potential role of gut microorganisms in exerting an important role in the wellbeing of the host fish,” Austin and his group conclude. The organism “stimulated both cellular and humoral immune responses, which may have provided the rainbow trout with adequate protection to survive the challenge by the highly virulent Aeromonas sp.” Studies conducted elsewhere have demonstrated that a closely related B. subtilis shows antibiosis against pathogenic vibrios. It has also been used to improve pond water quality, leading to increased survival of black tiger prawns. An alternative approach to the control of fish pathogens is, of course, immunization. But the difficulties inherent in their development can be gauged from recent, painstaking progress in studying a genus, Moritella, that is taxonomically remote from Aeromonas and other bacterial fish pathogens. The psychrophile M. viscosa is a particular target as the cause of winter ulcers in fish raised in sea cages below 10oC. Endemic in farmed salmonids in North Atlantic countries, the disease causes significant mortality and thus financial losses. Cod is vulnerable, as is turbot, though halibut is relatively resistant. A polyvalent vaccine has been on the market for several years, and has reduced the frequency of the disease. However, there is still considerable room for improvement. Yet the route towards a more potent and specific vaccine has been bedeviled by an elementary difficulty—the sensitivity of the bacterium to lysis—that reminds us how far fish microbiology has lagged behind other sectors of the subject until comparatively recently. Whereas the fragility of Neisseria gonorrhoeae and Streptococcus pneumoniae has been recognized for many years, and their autolytic enzymes thus intensively investigated, far less is known concerning those enzymes in marine bacteria. Two researchers who are now tackling this issue are Eva Benediktsdottir and Karen Heidarsdottir at the University of Iceland in Reykjavik. According to a recent report in Letters in Applied Microbiology (45:115–120, 2007), their work so far should not only facilitate the manufacture of an effective vaccine but also throw light on the pathogenicity of M. viscosa. Their meticulous studies have confirmed the environmental factors responsible for the premature lysis of the bacterial cells, and defined the composition of the medium and the temperature which minimize lysis and guarantee successful culture. Probably the most important single advance in fish pathology over the past year has been the delineation of the complete genome sequence of Flavobacterium psychrophilum by Eric Duchaud and colleagues in several different laboratories in France. Causing extensive necrosis known as “cold-water disease” in mature fish and a lethal hemorrhagic septicemia in young fish, F. psychrophilium is responsible for considerable economic losses in all major areas of salmonid aquaculture. There is no specific vaccine, and antibiotics do not offer a satisfactory method of control. However, as described in Nature Biotechnology (25:763– 769, 2007), the French research is expected to lead to major advances in understanding the molecular pathogenesis of the infection and thus the development of efficient disease control strategies. Though the tiny crustaceans called sea lice have been in the news recently for their attacks on wild and farmed salmon in British Columbia, it is bacteria, closely followed by oomycetes such as Saprolegnia, that inflict the greatest economic harm on aquaculture worldwide. Notwithstanding progress in biological control and other techniques, genome sequencing seems likely to provide the wherewithal for substantial advances in the future. Volume 3, Number 3, 2008 / Microbe Y 109