Interactions between accumulated copper, bacterial community structure and histamine levels in crayfish meat during storage.

BACKGROUND Pollution in aquaculture areas may negatively impact edible species and threaten seafood quality and safety. The aim of this study was to determine the interaction between copper and bacteria in the aquatic habitat and their impact upon crustaceans. Marbled crayfish was chosen as a model of aquatic crustaceans and the influence of metal contamination on bacterial community structure in water used to culture crayfish and in crayfish themselves was investigated. Histamine, an allergen commonly formed by certain groups of bacteria in crustacean edible tissue during storage, was also determined. RESULTS Copper exposure increased its concentration in crayfish meat by 17.4%, but the copper concentration remained within acceptable food safety limits. Elevated copper levels affected the bacterial community both in the water used to cultivate crayfish and in the marbled crayfish themselves. Cluster analysis of 16S rRNA-gene based microbial community fingerprints revealed that copper impacted the bacterial community in the water and in the crayfish meat. However, copper exposure reduced the formation of histamine in crayfish meat during storage by 66.3%. CONCLUSION Copper from the habitat appears to reduce histamine accumulation in crayfish meat during storage by affecting the bacterial community structure of the cultivation water and most likely also in the intestine of the crayfish. From a food safety point of view, copper treatment during the aqua culturing of crustaceans has a positive impact on the postharvest stage.

[1]  I. Roessink,et al.  Effect of copper exposure on histamine concentrations in the marbled crayfish (Procambarus fallax forma virginalis) , 2013 .

[2]  I. Roessink,et al.  Copper kinetics and internal distribution in the marbled crayfish (Procambarus sp.). , 2012, Chemosphere.

[3]  J. Macan,et al.  Determination of Biogenic Amines and Endotoxin in Squid, Musky Octopus, Norway Lobster, and Mussel Stored at Room Temperature , 2010, Arhiv za higijenu rada i toksikologiju.

[4]  A. Bianchini,et al.  Copper accumulation and toxicity in isolated cells from gills and hepatopancreas of the blue crab (Callinectes sapidus) , 2009, Environmental toxicology and chemistry.

[5]  M. Ferrer.  The microbial reactome , 2009, Microbial biotechnology.

[6]  A. T. Lombardi,et al.  The effects of humic substances on copper toxicity to Ceriodaphnia silvestrii Daday (Crustacea, Cladocera) , 2008, Ecotoxicology.

[7]  U. García,et al.  Histamine operates Cl–-gated channels in crayfish neurosecretory cells , 2007, Journal of Experimental Biology.

[8]  G. Scholtz,et al.  The parthenogenetic Marmorkrebs (marbled crayfish) produces genetically uniform offspring , 2007, Naturwissenschaften.

[9]  K. Schiff,et al.  Extent and magnitude of copper contamination in marinas of the San Diego region, California, USA. , 2007, Marine pollution bulletin.

[10]  U. Güner.  Freshwater crayfish Astacus leptodactylus (Eschscholtz, 1823) accumulates and depurates copper , 2007 .

[11]  M. Ferrer,et al.  Mining genomes and 'metagenomes' for novel catalysts. , 2005, Current opinion in biotechnology.

[12]  M. Coton,et al.  Multiplex PCR for colony direct detection of Gram-positive histamine- and tyramine-producing bacteria. , 2005, Journal of microbiological methods.

[13]  Jo Handelsman,et al.  Metagenomics or Megagenomics? , 2005, Nature Reviews Microbiology.

[14]  J. Dolfing,et al.  Inhibitory effects of copper on bacteria related to the free ion concentration , 1979, Microbial Ecology.

[15]  D. Hwang,et al.  Histamine-related hygienic qualities and bacteria found in popular commercial scombroid fish fillets in Taiwan. , 2004, Journal of food protection.

[16]  J. Castilla,et al.  Copper, copper mine tailings and their effect on marine algae in Northern Chile , 1999, Journal of Applied Phycology.

[17]  P. Vasseur,et al.  Performances of three bacterial assays in toxicity assessment , 1989, Hydrobiologia.

[18]  P. Rainbow,et al.  Comparative strategies of heavy metal accumulation by crustaceans: zinc, copper and cadmium in a decapod, an amphipod and a barnacle , 1989, Hydrobiologia.

[19]  H. W. van Verseveld,et al.  Section 7 update: Cluster analysis and statistical comparison of molecular community profile data , 2004 .

[20]  B. Kimura,et al.  Cloning and Sequencing of the Histidine Decarboxylase Genes of Gram-Negative, Histamine-Producing Bacteria and Their Application in Detection and Identification of These Organisms in Fish , 2003, Applied and Environmental Microbiology.

[21]  J. Kirby,et al.  Selenium, Cadmium, Copper, and Zinc Concentrations in Sediments and Mullet (Mugil cephalus) from the Southern Basin of Lake Macquarie, NSW, Australia , 2001, Archives of environmental contamination and toxicology.

[22]  F. Feldhusen.  The role of seafood in bacterial foodborne diseases. , 2000, Microbes and infection.

[23]  P. Matthiessen,et al.  Sources and Potential Effects of Copper and Zinc Concentrations in the Estuarine Waters of Essex and Suffolk, United Kingdom , 1999 .

[24]  H. An,et al.  Histamine Formation and Bacterial Spoilage of Albacore Harvested off the U.S. Northwest Coast , 1999 .

[25]  J. Šyvokienė,et al.  The Effect of Heavy Metals on Microorganisms of Digestive Tract of Crayfish , 1999 .

[26]  Julián García,et al.  Effects of copper and zinc on the activated sludge bacteria growth kinetics , 1998 .

[27]  B. Simpson,et al.  Enzymatic hydrolysis of shrimp meat , 1998 .

[28]  M. Fingerman,et al.  Metal accumulation in crayfish, Procambarus clarkii, exposed to a petroleum-contaminated Bayou in Louisiana. , 1997, Ecotoxicology and environmental safety.

[29]  H. N. Chinivasagam,et al.  Spoilage pattern of five species of Australian prawns: Deterioration is influenced by environment of capture and mode of storage , 1996 .

[30]  F. Gutiérrez-Corona,et al.  Copper resistance mechanisms in bacteria and fungi. , 1994, FEMS microbiology reviews.

[31]  A. Roig-Sagués,et al.  Bacteriological Quality of Tuna Fish ( Thunnus thynnus ) Destined for Canning: Effect of Tuna Handling on Presence of Histidine Decarboxylase Bacteria and Histamine Level. , 1994, Journal of food protection.

[32]  W. Admiraal,et al.  The contribution of complexed copper to the metabolic inhibition of algae and bacteria in synthetic media and river water , 1994 .

[33]  A. Uitterlinden,et al.  Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA , 1993, Applied and environmental microbiology.

[34]  H. R. Azad,et al.  Accumulation of Copper and Other Metals by Copper-Resistant Plant-Pathogenic and Saprophytic Pseudomonads , 1992, Applied and environmental microbiology.

[35]  N. Brown,et al.  Copper resistance determinants in bacteria. , 1992, Plasmid.

[36]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[37]  C. Lim,et al.  Copper Resistance Gene Homologs in Pathogenic and Saprophytic Bacterial Species from Tomato , 1990, Applied and environmental microbiology.

[38]  S. Nightingale.  Seafood safety. , 1990, American family physician.

[39]  J. Trevors,et al.  Copper toxicity and chemistry in the environment: a review , 1989 .

[40]  J. Timbrell.  Introduction to Toxicology , 1989 .

[41]  R. Jonas.  Acute Copper and Cupric Ion Toxicity in an Estuarine Microbial Community , 1989, Applied and environmental microbiology.

[42]  Steve L. Taylor,et al.  Histamine poisoning (scombroid fish poisoning): an allergy-like intoxication. , 1989, Journal of toxicology. Clinical toxicology.

[43]  C. Bender,et al.  Molecular cloning of copper resistance genes from Pseudomonas syringae pv. tomato , 1987, Journal of bacteriology.

[44]  W. Maher.  Trace metal concentrations in marine organisms from St. Vincent Gulf, South Australia , 1986 .

[45]  C. Bender,et al.  Indigenous plasmids in Pseudomonas syringae pv. tomato: conjugative transfer and role in copper resistance , 1986, Journal of bacteriology.

[46]  Jeffrey B. Jones,et al.  Linkage of copper resistance and avirulence loci on a self-transmissible plasmid in Xanthomonas campestris pv. vesicatoria , 1986 .

[47]  E. H. Marth,et al.  Histamine Production by Psychrotrophic Pseudomonads Isolated from Tuna Fish. , 1984, Journal of food protection.

[48]  C. F. Niven,et al.  Differential plating medium for quantitative detection of histamine-producing bacteria , 1981, Applied and environmental microbiology.

[49]  G. Hall,et al.  Copper toxicity: evidence for the conversion of cupric to cuprous copper in vivo under anaerobic conditions. , 1976, Chemico-biological interactions.