What is Biomphalaria glabrata? - Biology

What is Biomphalaria glabrata?
Biomphalaria glabrata is a mollusc and thus represents the lophotrochozoan clade of animal
life. It is a tropical freshwater snail indigenous to ponds, marshes and streams of South
America and some of the Caribbean islands. It is an important intermediate host of the
parasite Schistosoma mansoni that infects ~83 million people.

An Overview of Animal Phylogeny
CHORDATA
HEMICHORDATA
ECHINODERMATA
ARTHROPODA
TARDIGRADA
ONYCHOPHORA
NEMATODA
NEMATOMORPHA
PRIAPULIDA
KINORHYNCHA
BRYOZOA
BRACHIOPODA
PHORONIDA
ANNELIDA
MOLLUSCA
SIPUNCULIDA
PLATYHELMINTHS
PLACOZOA
CNIDARIA
PORIFERA
DEUTEROSTOMES
ECDYSOZOANS
LOPHO-
TROCHOZOANS
NO
LOPHO-
TROCHOZOAN
IS A “MODEL
ORGANISM”
Tree Modified from Conway Morris (1998) and Valentine et al., 1999

Phylum Mollusca
• >50 thousand living species
• Includes the largest and the most intelligent invertebrates
• Of commercial and public health importance
• Understudied with respect to genome sciences
250
70
600
11
8000
350
650
>40,000
SOLENOGASTERS (shell-less, worm-like molluscs)
CAUDOFAUVEATA (shell-less worm-like molluscs)
POLYPLACOPHORA (the chitons)
MONOPLACOPHORA (rare deep sea molluscs)
BIVALVIA (clams, oysters, scallops)
SCAPHOPODA (tusk shells)
CEPHALOPODA (chambered nautilus, squids, octopuses)
GASTROPODA (snails, slugs, sea hares, abalones)
A plausible scenario for the phylogenetic relationships among the major groups of molluscs (see Medina and Collins, 2003;
Passamaneck et al., 2004 for discussions).

Class Gastropoda
• >40 thousand living species of snails
• ancient origins, in the Cambrian
• B. glabrata is a relatively derived gastropod
A plausible scenario of relationships among gastropods (see Medina and Collins, 2003; Passamaneck et al., 2004 for discussions).
Note the family Planorbidae shown in red, to which B. glabrata belongs.

FAMILY PLANORBIDAE
• About 40 genera
• Cosmopolitan, in almost
any lake, pond or stream
• Shell often discoidal
• Animals with accessory
“gill” called a
pseudobranch
• Hemolymph is red due to
the presence of
hemoglobin
• Are frequently important
hosts for schistosomes,
including species other
than S. mansoni
(From Malek, 1985)
Adult Schistosoma bovis worms, from
cattle in Kenya, transmitted by another
planorbid snail genus, Bulinus.

• About 34 species, in tropical
America, Africa and the Arabian
Peninsula
• Originated in the Neotropics
and an ancestral snail very
much like B. glabrata colonized
Africa less than 5 million years
ago ( see * on tree)
• 18 species are known or likely
hosts for S. mansoni, a parasite
that originated in Africa
• B. glabrata is the most
important host in the Neotropics
23 SPECIES, PARTIAL MITOCHONDRIAL
16S AND COMPLETE NUCLEAR
RIBOSOMAL ITS1 AND 2
The genus Biomphalaria
10
*
pfeifferi Senegal
stanleyi Uganda*
pfeifferi Cameroon
pfeifferi Sudan
pfeifferi Madagascar
camerunensis 1999 Cameroon
camerunensis 2000 Cameroon
sudanica Kenya
sudanica Tanzania
choanomphala Tanzania*
alexandrina 1997 Egypt
alexandrina 1993 Egypt
smithi Uganda*
glabrata Dominican Republic
glabrata Puerto Rico
glabrata Brazil
glabrata Venezuela
kuhniana Dominica
kuhniana Colombia
kuhniana Venezuela
straminea PE Brazil
straminea SP Brazil
intermedia Paraguay
amazonica AM Brazil
amazonica RO Brazil
B. sp. Bolivia
tenagophila Paraguay
tenagophila Brazil
occidentalis Brazil
prona LkV, Venezuela*
prona SaC, Venezuela
andecola Bolivia
B. sp. (havanensis? HbL, Cuba
B. sp. (havanensis?) Zf, Cuba
B. sp (havanensis?) Puerto Rico
temascalensis Mexico*
obstructa USA
obstructa Mexico*
helophila
peregrina Uruguay
peregrina Brazil
Cuba
schrammi Brazil
Helisoma trivolvis USA
DeJong et al., 2001
AFRICAN
NEOTROPICAL

Variation within Biomphalaria glabrata
• There are 6 well-delineated clades within B. glabrata, four from geographically
overlapping areas in Brazil
• These are ~4X more diverse genetically than the most important intermediate
host for S. mansoni in Africa, Biomphalaria pfeifferi
*BB02 isolate selected
for sequencing from
this clade
Based on partial 16S and ND-1 sequences of the mitochondrial genome, DeJong et al., 2003.
*

Ecology of Biomphalaria glabrata
A small, heavily-polluted stream near Belo
Horizonte, Brazil, that harbored thriving
populations of B. glabrata, here being collected
with a small scoop. This habitat is a
transmission site for Schistosoma mansoni.
A pond in Brazil where
B. glabrata is present.
A Venezuelan pond in which B. glabrata
was abundant (note the many whitened
shells of dead snails that have floated to
the surface).
• Eat bacterial films, algae, diatoms and decaying macrophytes
• B. glabrata can live for 18-24 months in the laboratory, 15-18 months in field
• Under ideal conditions seven generations can be completed in a year
• One snail can produce 14,000 eggs in its life span
• B. glabrata can survive several months out of water, in aestivation, even at
high surrounding temperatures
• It has been introduced into Egypt and reported from the Nile Delta

Tools to Study the Biology of
Biomphalaria glabrata
• A BAC Library (Adema et al, 200X, in press)
• Microarrays
• EST projects underway
• Bge cell line
• ability to culture S. mansoni larvae with Bge
cells
• Availability of inbred lines susceptible or resistant
to S. mansoni
• RNAi being developed (Jiang et al., 200X, in
press)

Some Immunological Features of Biomphalaria glabrata
(From Lie et al., 1975)
They have a distinct
hematopoietic organ that
responds to infection with
pathogens, like trematodes.
Hemocytes attack and destroy
the tegument of parasites,
killing them in 2-4 days.
(From Lie et al., 1975)
This organ releases circulating
blood cells called hemocytes
into the circulation.
Hemocytes can also
collaborate to encapsulate
larger foreign objects like
trematode larvae.
A view of hemocytes spread
on a glass surface.
Hemocytes play an important
role in phagocytosis of foreign
objects.
Parasites can suppress these responses. How?

The Genome of Biomphalaria glabrata
• B. glabrata has a haploid number of
18 chromosomes, all of which are
relatively small and monomorphic
• 15 metacentric, 2 submetacentric,
1 subtelocentric
• The haploid genome size as
assessed by Feulgen image analysis
densitometry of B. glabrata was
estimated at 931 Mb (Gregory, 2003).
• B. glabrata has one of the smallest
known molluscan genomes
• these range from 0.4 to 5.9 pg
• The mitochondrial genome of B.
glabrata is known (13,670 nt)
• relatively small as gastropod
mitochondrial genomes are
concerned
Karyotype of Biomphalaria glabrata, NIH
strain 6-4-1. Goldman et al., 1983.
Mitochondrial genome of Biomphalaria
glabrata, M line strain. DeJong et al.,
2005.

Notable Features of the Biology of Biomphalaria glabrata
Relative to Other Organisms with Sequenced Genomes
• Produces a calcareous shell (biomineralization)
• Moist, mucus-covered, ciliated epithelium in
contact with the environment
• complex glycoproteins in mucus
(From Malek, 1985)
• Hermaphroditic, capable of self-fertilization
• parasites routinely cause castration
• Presence of numerous fibrinogen-encoding genes
• Now known to be present in other invertebrates
(tunicates, horseshoe crabs, spiders,
mosquitoes, flies)
• B. glabrata has the ability to produce
diversified fibrinogen-encoding proteins (FREPs)
• Ability to mount heightened secondary defense
(Malek, 1985)
responses to relevant pathogens
• Ability to tolerate allografts and even xenografts

The male with its
gynecophoric
canal
“the bun”
The female
residing within
the gynecophoric
canal
“the hot dog”
A Quick Review Of Schistosomes
1 mm
• They are flatworms (Phylum
Platyhelminthes) known as digenetic
trematodes or flukes.
• There are about 100 species in 13 genera,
of schistosomes.
• They are the most intensively studied of all
flatworms.
• They are unusual for being dioecious.
• The word “schisto-some” or “split body”
refers to gynecophoric canal of male in which
the female worm resides.
• Schistosomes live within the vertebrate
vascular system so are called “blood flukes.”
• Their complex life cycle is dependent on
snails.
• These worms infect about 200 million
people and 165 million cattle.

The Life Cycle of Schistosoma mansoni
Cercariae
released
into water
Cercariae
produced
in the snail
digestive
gland
Cercariae
penetrate
human skin
Asexual reproduction
occurs in freshwater
Snails of the genus
Biomphalaria
Adult worms
develop in
mesenteric
veins
MALE
FEMALE
Spined
eggs
passed in
the feces
Miracidium
hatches
from egg in
freshwater,
penetrates snail

ORGAN DAMAGE DUE TO SCHISTOSOMES
Damage caused by Schistosoma mansoni, a causative agent of human intestinal
schistosomiasis. Much of the damage is due to deposition of schistosome eggs in the
tissues.
Spined
egg causing
granuloma
This histological section of a liver shows an individual granuloma response. Notice the
large area of disruption of the normal liver architecture. Sitting at the center of the
granuloma is the item that incited its formation, a single schistosome egg.

The Distribution of Schistosoma mansoni
Mirrors That of its Snail Hosts
(From DeJong et al., 2003) (From WHO #728, 1985)
Biomphalaria glabrata Schistosoma mansoni

Is Schistosomiasis Relevant to the Developed World?
Yes! Although we are conditioned to think of schistosomiasis
as an exotic tropical malady, in reality every summer,
thousands of Americans become infected with schistosome
cercariae while engaged in recreational activities in our
natural waterbodies. This snail-transmitted condition,
particularly well-known to residents of northern mid-western
states, is called swimmer’s itch or cercarial dermatitis.
Infection results in a raised itchy red papule on the skin that
takes several days to resolve; in some cases hundreds of
such papules may occur on the skin of an individual victim.
The parasites responsible are poorly-characterized yet
ubiquitous schistosomes of several species that have natural
cycles of transmission involving aquatic birds and snails.
Although neither life-threatening nor contagious, this
condition nonetheless merits new attention for several
reasons. Cercariae of some avian schistosomes are not
inevitably killed in mammalian skin but can undertake visceral
or neurotropic migrations.
See NATURE (Vol 436 4 August 2005) for a discussion of a
recent outbreak of dermatitis in San Francisco Bay involving
the cercaria shown to the right. Dr. Sara Brant was
instrumental in showing that the snail implicated in the
outbreak was a species exotic to the Bay.
DR. SARA BRANT