Histidine Decarboxylases and Their Role in Accumulation of Histamine in Tuna and Dried Saury

Abstract

Histamine-producing bacteria (HPB) such as Photobacterium phosphoreum and Raoultella planticola possess histidine decarboxylase (HDC), which converts histidine into histamine. Histamine fish poisoning (HFP) is attributable to the ingestion of fish containing high levels of histamine produced by HPB. Because freezing greatly decreases the histamine-producing ability of HPB, especially of P. phosphoreum, it has been speculated that HFP is caused by HDC itself from HPB cells autolyzing during frozen storage, even when HPB survive frozen storage. Here we constructed recombinant HDCs of P. phosphoreum, Photobacterium damselae, R. planticola, and Morganella morganii and investigated the ability of HDCs to produce sufficient histamine to cause HFP. To elucidate the character of these HDCs, we examined the specific activity of each recombinant HDC at various temperatures, pH levels, and NaCl concentrations. Further, we also investigated the stability of each HDC under different conditions (in reaction buffer, tuna, and dried saury) at various temperatures. P. damselae HDC readily produced sufficient histamine to cause HFP in fish samples. We consider that if HDC is implicated as an independent cause of HFP in frozen-thawed fish, the most likely causative agent is HDC of P. damselae.Histamine fish poisoning (HFP) is a food-borne chemical intoxication caused by the ingestion of histidine-rich scombroid fish such as tuna, bonito, and mackerel in which histamine-producing bacteria (HPB) produce a large amount of histamine (1,22). HPB isolated from fish implicated in actual HFP incidents reported to date include Raoultella planticola, Morganella morganii, Hafnia alvei, and Photobacterium phosphoreum (11,15). Enteric bacteria such as R. planticola and M. morganii are reported to be the dominant HPB in fish, whereas P. phosphoreum and Photobacterium damselae are frequently isolated from fish subjected to appropriate examination for marine bacteria, such as by the addition of NaCl to the culture medium and avoidance of exposure of the bacterium to high temperatures (11,16,17). The former is a psychrotrophic bacterium in the marine environment which has greater histamine-producing activity than enteric bacteria at low temperatures (11). The latter is also a prolific HPB but a mesophilic marine bacterium (13).It has been shown that accumulation of histamine by HPB occurs after the level of bacterial growth exceeds 10 7 CFU/ml in culture medium (19). Viable cell counts of P. phosphoreum and R. planticola have been reported to decrease during frozen storage (2,8). Moreover, the histidine-producing capability of HPB decreases due to injury from freezing, even if the HPB survive frozen storage (6, 21). Tuna, a scombroid fish frequently implicated in HFP, is commonly frozen during fishing and distribution (3). Other scombroid fish are also frequently frozen in current practice. These factors have led to speculation that the accumulation of histamine in thawed fish arises from the release of histidine decarboxylase (HDC) from the autol...

Biogenic amines, amino acids and microflora changes in Indian mackerel (Rastrellinger kanagurta) stored at ambient (25–29 °C) and ice temperature (0 °C)

“…This incubation temperature was selected for the growth of mesophilic microflora which is reported as a major amines former in literature. Temperature of 30-40°C was also shown to be optimum for histidine decarboxylase activity of several psychrotrophic microflora (Kanki et al 2007). As a limitation, this parameter is not favourable to the growth of psychrotrophic bacteria.…”

227 Effect of different cooking methods on histamine levels in selected foods

“…The formation of histamine in food requires the presence of histidine decarboxylase-positive microorganisms, in conjunction with conditions allowing the growth and enzyme activity of these bacteria 42 . It is known that there are several factors (e.g., pH, temperature, and NaCl concentration) that affect histidine decarboxylase activity 14,43,44 . This enzyme activity increased with increasing temperature to 30 o C∼40 o C and decreased above 50 o C. Although histidine decarboxylase activity decreased at high temperature, histamine production would continue until the enzyme became inactive 44 .…”

“…It is known that there are several factors (e.g., pH, temperature, and NaCl concentration) that affect histidine decarboxylase activity 14,43,44 . This enzyme activity increased with increasing temperature to 30 o C∼40 o C and decreased above 50 o C. Although histidine decarboxylase activity decreased at high temperature, histamine production would continue until the enzyme became inactive 44 . Histamine, once formed in food, is heat stable even if heating inactivates both the enzyme and the source microorganisms 21,34,35 .…”

Effect of Histamine-producing Bacteria on Fermented Fishery Products

“…In the case of raw fish, such as Scombroid fish, mainly gramnegative bacteria, Enterobacteriaceae, and Photobacterium spp., are known to produce histamine (EFSA, 2011;Emborg et al, 2006;FAO/WHO, 2012;Kanki et al, 2007;Lehane, 2000, Okuzumi et al, 1981Sato et al, 1994;Takahashi et al, 2003;Torido et al, 2012b). Histamine-producing Enterobacteriaceae include common enteric mesophiles, such as Morganella, Enterobacter, Hafnia, Raoultella, and others.…”

“…Two HDC isozymes are known as bacterial enzymes: pyridoxal phosphate (PLP)-dependent HDC in gram-negative bacteria and pyruvoyl-type HDC in grampositive bacteria (Landete et al, 2008). In the many PLP-dependent HDCs, the enzymes are constructed as a 170 kDa homotetramer, which is widely distributed in Enterobacteriaceae, Photobacterium spp, mammal liver, and others (Fujii et al, 1994;Kamath et al, 1991;Kanki et al, 2007;Morii et al, 2003;Tanase et al, 1985).…”