TY - JOUR
T1 - Poikilothermic Animals as a Previously Unrecognized Source of Fecal Indicator Bacteria in a Backwater Ecosystem of a Large River
AU - Frick, Christina
AU - Vierheilig, Julia
AU - Linke, Rita
AU - Savio, Domenico
AU - Zornig, Horst
AU - Antensteiner, Roswitha
AU - Baumgartner, Christian
AU - Bucher, Christian
AU - Blaschke, Alfred P
AU - Derx, Julia
AU - Kirschner, Alexander K T
AU - Ryzinska-Paier, Gabriela
AU - Mayer, René
AU - Seidl, Dagmar
AU - Nadiotis-Tsaka, Theodossia
AU - Sommer, Regina
AU - Farnleitner, Andreas H
N1 - Funding Information:
This paper was supported by the Austrian Science Fund (FWF) as part of the “Vienna Doctoral Program on Water Resource Systems” (W1219-N22), the FWF single project Unify (P23900-B22), and the research project “Groundwater Resource Systems Vienna,” in cooperation with Vienna Water as part of the “(New) Danube-Lower Lobau Network Project” (Gewässervernetzung [Neue] Donau-Untere Lobau [Nationalpark Donau-Auen]) funded by the Government of Austria (Federal Ministry of Agriculture, Forestry, Environment and Water Management), the Government of Vienna, and the European Agricultural Fund for Rural Development (project LE 07-13).
Publisher Copyright:
© 2018 American Society for Microbiology.
PY - 2018/8/1
Y1 - 2018/8/1
N2 - Quantitative information regarding the presence of Escherichia coli, intestinal enterococci, and Clostridium perfringens in poikilotherms is notably scarce. Therefore, this study was designed to allow a systematic comparison of the occurrence of these standard fecal indicator bacteria (SFIB) in the excreta of wild homeothermic (ruminants, boars, carnivores, and birds) and poikilothermic (earthworms, gastropods, frogs, and fish) animals inhabiting an alluvial backwater area in eastern Austria. With the exception of earthworms, the average concentrations of E. coli and enterococci in the excreta of poikilotherms were equal to or only slightly lower than those observed in homeothermic excreta and were 1 to 4 orders of magnitude higher than the levels observed in the ambient soils and sediments. Enterococci reached extraordinarily high concentrations in gastropods. Additional estimates of the daily excreted SFIB (E. coli and enterococcus) loads (DESL) further supported the importance of poikilotherms as potential pollution sources. The newly established DESL metric also allowed comparison to the standing stock of SFIB in the sediment and soil of the investigated area. In agreement with its biological characteristics, the highest concentrations of C. perfringens were observed in carnivores. In conclusion, the long-standing hypothesis that only humans and homeothermic animals are primary sources of SFIB is challenged by the results of this study. It may be necessary to extend the fecal indicator concept by additionally considering poikilotherms as potential important primary habitats of SFIB. Further studies in other geographical areas are needed to evaluate the general significance of our results. We hypothesize that the importance of poikilotherms as sources of SFIB is strongly correlated with the ambient temperature and would therefore be of increased significance in subtropical and tropical habitats and water resources.IMPORTANCE The current fecal indicator concept is based on the assumption that the standard fecal indicator bacteria (SFIB) Escherichia coli, intestinal enterococci, and Clostridium perfringens multiply significantly only in the guts of humans and other homeothermic animals and can therefore indicate fecal pollution and the potential presence of pathogens from those groups. The findings of the present study showed that SFIB can also occur in high concentrations in poikilothermic animals (i.e., animals with body temperatures that vary with the ambient environmental temperature, such as fish, frogs, and snails) in an alluvial backwater area in a temperate region, indicating that a reconsideration of this long-standing indicator paradigm is needed. This study suggests that poikilotherms must be considered to be potential primary sources of SFIB in future studies.
AB - Quantitative information regarding the presence of Escherichia coli, intestinal enterococci, and Clostridium perfringens in poikilotherms is notably scarce. Therefore, this study was designed to allow a systematic comparison of the occurrence of these standard fecal indicator bacteria (SFIB) in the excreta of wild homeothermic (ruminants, boars, carnivores, and birds) and poikilothermic (earthworms, gastropods, frogs, and fish) animals inhabiting an alluvial backwater area in eastern Austria. With the exception of earthworms, the average concentrations of E. coli and enterococci in the excreta of poikilotherms were equal to or only slightly lower than those observed in homeothermic excreta and were 1 to 4 orders of magnitude higher than the levels observed in the ambient soils and sediments. Enterococci reached extraordinarily high concentrations in gastropods. Additional estimates of the daily excreted SFIB (E. coli and enterococcus) loads (DESL) further supported the importance of poikilotherms as potential pollution sources. The newly established DESL metric also allowed comparison to the standing stock of SFIB in the sediment and soil of the investigated area. In agreement with its biological characteristics, the highest concentrations of C. perfringens were observed in carnivores. In conclusion, the long-standing hypothesis that only humans and homeothermic animals are primary sources of SFIB is challenged by the results of this study. It may be necessary to extend the fecal indicator concept by additionally considering poikilotherms as potential important primary habitats of SFIB. Further studies in other geographical areas are needed to evaluate the general significance of our results. We hypothesize that the importance of poikilotherms as sources of SFIB is strongly correlated with the ambient temperature and would therefore be of increased significance in subtropical and tropical habitats and water resources.IMPORTANCE The current fecal indicator concept is based on the assumption that the standard fecal indicator bacteria (SFIB) Escherichia coli, intestinal enterococci, and Clostridium perfringens multiply significantly only in the guts of humans and other homeothermic animals and can therefore indicate fecal pollution and the potential presence of pathogens from those groups. The findings of the present study showed that SFIB can also occur in high concentrations in poikilothermic animals (i.e., animals with body temperatures that vary with the ambient environmental temperature, such as fish, frogs, and snails) in an alluvial backwater area in a temperate region, indicating that a reconsideration of this long-standing indicator paradigm is needed. This study suggests that poikilotherms must be considered to be potential primary sources of SFIB in future studies.
KW - Animals
KW - Animals, Wild/microbiology
KW - Bacteria/isolation & purification
KW - Bacterial Physiological Phenomena
KW - Birds/microbiology
KW - Body Temperature Regulation
KW - Clostridium perfringens/isolation & purification
KW - Ecosystem
KW - Environmental Biomarkers
KW - Environmental Monitoring
KW - Escherichia coli/isolation & purification
KW - Feces/microbiology
KW - Oligochaeta/microbiology
KW - Rivers/microbiology
KW - Water Microbiology
KW - Mollusk
KW - Escherichia coli
KW - Clostridium perfringens
KW - Earthworm
KW - Fishes
KW - Poikilothermic
KW - Enterococci
KW - Frog
KW - Excreta
KW - Alluvial
UR - http://www.scopus.com/inward/record.url?scp=85051700489&partnerID=8YFLogxK
U2 - 10.1128/AEM.000715-18
DO - 10.1128/AEM.000715-18
M3 - Journal article
C2 - 29884761
SN - 0099-2240
VL - 84
JO - Applied and Environmental Microbiology
JF - Applied and Environmental Microbiology
IS - 16
M1 - e00715-18
ER -