Pergamon
PII: S0043-1354(96)00193-5
Wat. Res. Vol. 30, No. 11, pp. 2812-2816, 1996
Copyright © 1996ElsevierScienceLtd
Printed in Great Britain.All fights reserved
0043-1354/96$15.00 + 0.00
USEFULNESS OF BACTERIOPHAGES INFECTING
BACTEROIDES FRAGILIS AS INDEX MICROORGANISMS
OF REMOTE FAECAL POLLUTION
F. LUCENA, R. ARAUJO @ and J. JOFRE @*
Department of Microbiology, University of Barcelona, Avenida Diagonal 645, 08028 Barcelona, Spain
(First received August 1994; accepted in revised form June 1996)
Abstract--Levels of faecal bacteria, somatic coliphages and bacteriophages of Bacteroides fragilis were
counted in marine sediments and groundwater as representatives of environments with remote faecal
pollution. Additionally, enterovirus were measured in the marine sediments. Clear changes of the
proportions of the different microorganisms are observed when microbial numbers in groundwater and
marine sediments are compared to the numbers found in sewage or water recently polluted by sewage.
These changes show that phages of B. fragilis reach sites that receive persistent pollution more successfully
than somatic coliphages or indicator bacteria, with the exception of Clostridium perfringens. Multifactorial
analysis of marine sediments and groundwater data clustered phages, viruses and C. perfringens in one
factor and faecal bacteria in another. These data clearly suggest that Clostridium, phages of B. fragilis
and, in some cases enteroviruses, are better index microorganisms of remote faecal pollution than present
bacterial indicators. Copyright © 1996 Elsevier Science Ltd
Key words--bacteriophages, enterovirus, bacteria, Bacteroides fragilis, coliphages, indicators, faecal,
groundwater, sediments
INTRODUCTION
The sanitary quality of water is currently judged on
the basis of indicator bacteria. However these
bacteria may not reflect the quality of water regarding
other pathogens such as viruses and parasites
(Payment et al., 1991; Casemore, 1991). This lack of
correlation is especially significant in environmental
samples in which contaminant microorganisms had
suffered different inactivating processes, as for
example treated waters (Berg et al., 1978), ground-
water (Marzouk et al., 1980; Walter et al., 1982;
Vaughn et al., 1978), marine water (Lucena et al.,
1982) and shellfish (Goyal et al., 1979; Wait et al.,
1983). As a consequence, groundwater (Craun, 1979,
1991) and shellfish (Rippey, 1991) account for a very
large fraction of the documented waterborne
diseases, of which a very important fraction are of
viral origin (Keswick and Gerba, 1980; Rippey,
1991). Consequently, the need for good surrogate
indicators of viral pollution is widely recognised
(IAWPRC Study Group, 1991; Pancorbo and
Barnhart, 1992). Some bacteriophages infecting
enteric bacteria are being studied as potential
indicators of human viruses in the environment
(Tartera et al., 1987; Tartera et al., 1989; IAWPRC
Study Group, 1991).
We now present data on microbial loads in marine
*Author to whom all correspondence should be addressed
[Tel.: 3 93 402 14 83].
sediments and groundwater. In these environments
surviving faecal contaminants have undergone a
number of processes that reflect the different factors
that determine the occurrence of these organisms in
environments with remote faecal pollution. However,
in both cases we have selected rather polluted
sampling sites in order to obtain useful data. The
microorganisms studied are bacterial indicators
including C. perfringens and Aeromonas, somatic
coliphages, phages infecting B. fragilis and en-
teroviruses in some samples. Enteroviruses were not
counted in those samples that required a concen-
tration step.
MATERIALS AND METHODS
Sampling sites
Groundwater samples were collected at different sites
from a free alluvial aquifer belonging to the basin of Besos
river. Sampling stations were distributed over an area of
8 km2. The main influx of faecal pollution into the aquifer
is through infiltrated water from the Besos river, which is
heavily loaded with human faecal pollution. Mean microbial
loads per 100 ml of Besos fiver water in the area where this
study was performed were: total coliforms, 3.2 × 10% faecal
coliforms, 9.1 × 105; faecal streptococci, 1.9 x 105; C.
perfringens, 1.2 × 104; somatic coliphages, 1.7 × 105; and
bacteriophages infecting B. fragilis HSP40, 1.2 x 103.
Marine sediments were collected at distances of 300 m to
12 km from the shoreline and at water depths ranging from
6.5 m to 60 m in an area of around 25 km2 which was highly
influenced by different sources of pollution such as the Besos
river, the Llobregat river, treated domestic wastewater,
some minor sewage outfaUs and dumping of sewage sludge.
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