8/17/2019 Microbial taphnomy of archaeological bone
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Microbial Taphonomy of Archaeological Bone
Author(s): A. M. ChildReviewed work(s):Source: Studies in Conservation, Vol. 40, No. 1 (Feb., 1995), pp. 19-30Published by: International Institute for Conservation of Historic and Artistic WorksStable URL: http://www.jstor.org/stable/1506608 .
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8/17/2019 Microbial taphnomy of archaeological bone
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MICROBIALTAPHONOMY
OF
ARCHAEOLOGICAL
BONE
A.M.
Child
Summary-Taphonomy
is the
study
of
all
changes
that occur within an animal or
plant following
death. Bone
is
the
predominant
material
of
animal
origin
to
survive within the
archaeological
environment.It
is the
source
of
a
wealth
of information concerning
the
relationships,
diets,
disease and
ages
of people
(and
animals)
in
past
cultures. For this
information
to
be extracted
and
interpreted,
there
is
a need
for
conservators
and
archaeological
scientists to be aware
of
the
processes
of
taphonomic change
which
may
occur
in
bone.
These
changes
are
legion;
this
paper
attempts
to
define
some
of
the
major changes
seen in bone
which
may
be
attrib-
utable to the various
actions
of microorganisms.
Introduction
Taphonomy
is the
study
of all
changes
occurring
within
a substrate
following
death. These
changes
are many and varied, and it is not the aim of this
article to
present
a
comprehensive
list. The main
factors involved
in
the
taphonomic
changes
of
bone
in
the
burial environment
will be discussed
below.
Bone is the
predominant
material of animal ori-
gin
to survive within
the
archaeological
environ-
ment. It
is
a
composite
material,
comprising
both
inorganic
and
organic
fractions. Its
study
reveals
considerable
information to
the
conservator,
the
bone
specialist
and the
archaeological
scientist. For
this
information
to be
retrieved,
the conservator
must be aware of
the
likely
mechanisms
of
decom-
position
and
the
state of
preservation
of
the exca-
vated bone.
One
of the
major
problems
confronting analysts
and
conservators of
archaeological
bone is the
assessment of its
integrity,
since
conservation
treat-
ments will be
dictated
by
degree
of
preservation.
Both the
inorganic
and
the
organic phases
of bone
can be
changed
by taphonomic
processes,
and esti-
mation of the
degree
of
preservation
of
these
phases
based
upon
external
morphology
has
been
proved
to
be unreliable
[1].
Definitions
For
clarity,
some
of
the
terms
used
in
this
paper
have been defined here. Other definitions exist,
however;
the
definitions
given
here have
been
selected because
they
represent
the
most common
usage.
Biodegradation:
any
change
in the
properties
of
a
material
caused
by
the
activities of
organisms.
Received
30
June 1993
Received in revised
orm
22
August
1994
Studies in
Conservation40
(1995)
19-30
Biodeterioration:
any
undesirable
change
in
the
properties
of a
material
caused
by
the activities
of
organisms [2].
Biostratinomy:
changes
occurring
in an
animal
or
plant
after death
but before
burial
[3].
Diagenesis:
changes occurring
in
the
animal or
plant following
death
and
burial
[3].
Microbial
decomposition:
deleterious
changes
to
a
substrate
due to
the action of
microorganisms,
their
metabolic
by-products
and their
enzymes.
Bone structure
Bone is a highly specialized composite material
comprising
both
inorganic
(mineral)
and
organic
(mostly
protein) phases.
Its
inorganic
fraction
(90 )
is calcium
hydroxyapatite.
The
remaining
10
is
organic,
made
up
of
collagen,
non-collagenous
pro-
teins
(NCP),
lipids,
mucopolysaccharides
and
other
carbohydrates
[4].
There are
two
types
of
bone,
cancellous
bone
(spongy
bone)
and
compact
bone
(cortical
bone),
and their
distribution within
the
body
is dictated
by
biomechanical
considerations.
Both
compact
and
cancellous bone
are
formed
by
the
deposition
of
collagen
fibrils
in
layers.
In
com-
pact
bone,
these
layers
are laid
down in
rings
around the osteone, their alignment changing by
approximately
90? in
each
layer [5].
Bone mineral
Hydroxyapatite, Ca10(PO4)6(OH)2,
s the
basis of
the
inorganic component
of
bone.
Bone
mineral
is
a
complex
substance,
not
stoichiometric with
respect
to
hydroxyapatite.
Its
calcium to
phosphorus
ratio
is
significantly
less than
10:6,
so
that the
apatite
requires,
in
addition to its
calcium,
phosphate
and
hydroxy
ions,
substantial
amounts of
carbonate and
19
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A.M.
Child
lesser
quantities
of
pyrophosphate, magnesium,
sodium and
potassium
[6].
Strontium and
lead,
ingested
as
part
of the diet of
an
individual,
are
stored in the
skeleton. Fluoride ions have a
high
affinity
for
bone
mineral,
converting hydroxyapatite
to
fluorapatite,
and
fluoride
analyses
have been
used to check
provenance [7].
Bone
proteins
The
organic
fraction of bone
comprises
10-15
of
the total bone
weight.
There is one
major protein
component,
collagen,
and
a
group
of
proteins
termed
collectively
non-collagenous protein
(NCP).
Collagen
The
collagen
triple-helix
is
present
in
abundance
in
a
range
of
different
vertebrate tissues. Thirteen dif-
ferent
collagen
types
have been
described,
varying
in their chain composition and amino acid sequence
[8].
The
collagen present
in bone is
Type
I,
which
comprises
two
chains of one
composition,
al(I),
and one of
another,
a2(I).
Bone
collagen
has
an
average composition
of 30
glycine,
14
proline
and 11
hydroxyproline,
the remainder
making up
less than half the
total amino acids
[9]. Collagen
is
the
only
human
protein
in
which
hydroxyproline
occurs
in
significant
amounts;
this amino acid
restricts the
action of
proteases
[10].
In
the
Type
I
collagen
molecule,
the
protein
chains are
approxi-
mately
1000 amino acids
(residues) long
with
glycine
(the
smallest amino
acid) occurring every
third residue to give the dominant sequence:
glycine-proline-hydroxyproline
Because
of
the
presence
of
glycine
residues,
the col-
lagen
chains
are
tightly
twisted;
chains
which
are
tightly
twisted have an
increased resistance
to the
action of
proteolytic
enzymes.
The chains contain
hydrogen
bonds between
the amide
nitrogen
of
glycine
in
one chain
and the
non-glycine
carboxyl
oxygen
in
an
adjacent
chain
[11].
Mature
Type
I
collagen
is further
strengthened by
a covalent bond
which forms between
lysyl
amino acid
[12].
This
covalent bond
is
peculiar
to bone
collagen,
and
makes the molecule even more resistant to enzy-
matic
cleavage
and
laboratory
extraction
proce-
dures.
The
presence
of the
mineral,
which is
in
intimate association
with the
collagen,
further
inhibits the
access and action
of
enzymes.
Non-collagenous
proteins
Non-collagenous proteins
(NCP)
are a
complex
group.
Bone contains
two sources of
NCP,
one
arising
from outside the bone
(i.e.,
a-2HS-glycopro-
tein and
albumin)
and
the other from the bone
itself
(i.e.,
osteonectin
and
osteocalcin).
Osteonectin
is
thought
to be
involved
in the
deposition
and
development
of
primary
bone
tissue,
and osteocal-
cin is concerned
with
the
remodelling
and
develop-
ment of
secondary
bone tissue. The
bone-specific
NCPs
are
high
in
aspartic
and
ycarboxyglutamic
acid
residues
[13].
Bone as
an
archaeological
resource
As stated
above,
bone
is
the
predominant
material
of animal
origin
to survive
within the
archaeologi-
cal environment.
Its
study
reveals considerable
information
to the
conservator,
the bone
specialist
and the
archaeological
scientist.
Archaeological
skeletal materials
provide
two avenues
of
investiga-
tion:
palaeopathology
and
archaeological
science.
Palaeopathology
The gross morphology of archaeological bone can
be
changed
by
the burial
environment,
but
physical
measurements of skeletal bone
dimensions will still
yield
information on
growth,
health and incidence
of some diseases
within human
populations.
Similar
examination
of animal bone
produces
information
relating
to
butchering
methods,
diet,
hunting
and/or
farming techniques practised by
ancient
populations
[14]. Microscopic
examination of
archaeological
bone
(and
the related
surviving
soft
tissues)
will
yield
more information
on
disease
[15].
Archaeological
science
The preservation of bone depends not upon the
length
of burial
but
upon
the environment
of bur-
ial.
If
bones
are
sufficiently well-preserved,
they
still
contain
indigenous organic
macromolecules.
These
can be used
to
provide
information
on:
-the
age
of
the bone
by
radiocarbon
dating
[16-18]
or
by
amino acid racemization
[19-22];
-the diet of
the
animal
by
stable
isotope
analysis
[23-26];
-genetic relationships
[27-29].
This information
is
only
reliable where
the
proteins
used have survived unchanged by biological, physi-
cal or chemical
degradative
processes [30].
Survival
of
proteins
in
archaeological
bone
This
article is restricted
to a discussion of
the
effects
on bone
of the microbes within
terrestrial
environments.
It
is assumed here
that the bone
(with
or
without
flesh)
enters
the burial environ-
ment
in
direct
contact
with the
soil,
and is not
buffered
by
the
presence
of a
coffin,
shroud
or
other
protective layer.
Studies n Conservation0 (1995)19-300
8/17/2019 Microbial taphnomy of archaeological bone
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Microbial
aphonomy
f
archaeological
one
Bone
protein
is
unusual
in that
it survives over
archaeological,
even
geological,
time scales.
Generally, protein
loss
from
unmineralized sub-
strates
is
considered to be
exponential,
so that the
amount
which
survives
depends
upon
the initial
concentration
[31].
The
protein
loss within archaeo-
logical
bone does not follow this
pattern
and,
as a
result,
archaeological
bone can contain
only
1-2
nitrogen
[26].
Indeed,
the
carbon to
nitrogen
ratio
in
archaeological
bone
collagen
does
not
change
from that of modem bone
until almost all
of
the
collagen
(97 )
has been lost
[23].
Where 98
of
the
original
bone
protein
has been
lost,
the amino
acid content is
enriched
in
aspartic
and
glutamic
acid residues
[26,
32].
The
original
source of
these
residues is
uncertain; however,
three
possibilities
exist:
-contamination of the bone
proteins
with soil
pro-
teins [33];
-survival of
the
NCP,
rich
in these
residues,
whose
presence
is
masked
when
collagen
survives
well
[32];
-selective
decomposition
of the
collagen
helix,
to
leave acidic amino acids of
collagen
origin.
The
degree
to which
proteins
survive intact in
bones
from
archaeological
contexts
can be
mea-
sured
using
immunochemical means.
Although
these
methods are well
established
for
application
to
modem
materials,
they
have
only recently
been
applied
to
archaeological
ones
[34-39].
Results must
be viewed with caution [40]; however,
they
show
that
indigenous proteins (i.e.,
apohaemoglobin
and
osteocalcin)
survive in
an
immunologically recog-
nizable form in bones.
Proteins
(both
collagens
and
NCP)
are
thought
to
survive
in bone
because
of
their close association
with the mineral
phase,
which
protects
against
enzyme
attack.
The
collagens
are
further
preserved
because
of their
innately protective
structure and
chemistry
(see
'Collagen'
above).
Dissolution of the
bone mineral
The response of the mineral and organic phases of
bone to
the
burial
environment
will
differ.
Janaway
[41]
suggested
that
decomposition
of
bone
probably
occurs in the later
stages
of
the
decomposition
of a
corpse,
but this
is
not
likely.
Deterioration,
both
biochemical
(autolysis)
and
microbiological,
of tis-
sue
begins
immediately
after
death,
the
soft tissues
usually
showing
the
effects
first. If the
microbiologi-
cal
decomposition
of bone is inhibited
by
the
con-
tinued
presence
of the mineral
phase,
then the
degradation
of
collagen
will
proceed by
chemical
means
(see
below).
Dissolution due to
the soil
chemistry
The chemical and
physical
deteriorationof buried
bone
depends
solely
upon
the
chemistry
and
bio-
chemistry)
of the
surrounding
burial
environment.
Acidic
soils
will
dissolve
hydroxyapatite,
but the
thresholdof acidity required s not clear; at pH
<
5,
demineralization
s
promoted[42].
The rate of
dissolution
will
depend
on the
pH
of
the
soil,
the
concentration f
chelatingagents
and the
degree
of
water
percolation.
Bone tends to survive better in
soils with a
neutral or
very
slightly
alkaline
pH.
This
is
because
the bone mineral is
less
likely
to
dissolve,
but it must be
noted that soils low in
phosphate
will also
promote
demineralization
43].
Calcium
hydroxyapatite,
Ca10(PO4)6(OH)2,
can
be
changed
both
by
dissolution
and
recrystallization
and
by
hetero-ionic
substitution
(e.g.
Fe2+,
Ca2+).
Vivianite
(Fe3(PO4)2
8H20),
brushite
(CaHPO4)
and
calcite (CaCO3)will form within archaeological
bones
depending
upon
the
pH
and
chemistry
of
the
soil matrix.
Soils
high
in
Ca2+will
lead
to
the
break-up
of the
bone,
because
CaCO3,
ormed in
high-calcium
oils,
occupies
a
larger
space
than the
crystals
of
Ca10(PO4)6(OH)2.
The
presence
of
CaCO3
exerts internal
stresses within
the
bone
which will
result in
embrittlement and
cracking.
Internal
stresses
which
cause
damage
to the
gross
morphol-
ogy
of bone are
induced when bone is
exposed
to
alternating
wetting/drying
and
freezing/thawing.
These stresses are
aggravatedby
the
presence
of
soluble salts
[44].
Dissolution due
to microbial
decomposition
Generally,
n
well-aerated
oils,
the
decomposition
of
organic
matter is
rapid.
The
high
mineral
con-
tent of
bone,
however,
will
initially
inhibit the
microbial
decomposition
of
collagen.
This decom-
position
will
be
affected
by
the relative
numbers
constituting
the
microbial
population
of
different
soils.
The
composition
of the soil
microflora is
highly
dependent
upon
soil
pH,
and the
metabolic
activity
of
microorganisms
will
influence he
pH
of
the
soil,
especially
those
activities that involve
redox reactions[45]. The conditions which affect
the survivalof bone in the
archaeological
nviron-
ment
[46]
are
also
those
which will affect the
growth
and
survival
of
microorganisms
n the soil
[45,
47].
Microorganisms
will
penetrate
into bone
using
natural
spaces(e.g.
blood vessel
and nerve
acunae),
releasing
heir
enzymes
and
depositing
amino acids
[48, 49]. They
will
grow
using
the
surrounding
unmineralized
issues as a food
source and excrete
their
secondary
metabolites. The
nature of these
products
of
microbial
metabolismwill
dependupon
Studies n Conservation0 (1995)19-30 21
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A.M.
Child
the
environment
in
which
the
decomposition
occurred.
Anaerobic and aerobic
decomposition
Microorganisms
can be
divided into three cate-
gories, depending upon
their metabolism:
they may
be either
obligately
aerobic,
facultatively
anaerobic
or
obligately
anaerobic
[50].
In
aerobic
environments,
complete
decomposition
of the
protein
to
carbon
dioxide,
water,
nitrogen
dioxide and
sulphur
dioxide
occurs without
a
con-
siderable reduction
in
pH;
therefore the
proteins
in
bone are more
likely
to survive. All the
fungi
and
some of the bacteria have an
obligately
aerobic
metabolism,
degrading complex proteins
with
prote-
olytic
enzymes. Rapid
aerobic
growth
will
promote
anaerobic
conditions;
this
occurs when
the rate
of
oxygen consumption
exceeds the rate of
oxygen
dif-
fusion
into the
system.
When
anaerobic conditions
have been
achieved,
the
obligate
aerobic
microor-
ganisms
will
stop growing,
but the bacteria that
have the
facility
for both anaerobic and aerobic
decomposition
will switch
to
anaerobic
pathways.
The
obligate
anaerobes
will
start to flourish.
Anaerobic fermentation
uses
substances other
than molecular
oxygen
as a terminal electron
accep-
tor
[50].
Microbial
decomposition
of
protein
under
anaerobic conditions
leads,
initially,
to a
drop
in
pH.
This is due
to
the
generation
of
acidic com-
pounds
such as low molecular
weight
fatty
acids
and amino
acids,
which are
by-products
of
anaero-
bic
metabolism.
Their
presence
will result in the
demineralization of
hydroxyapatite
and the
expo-
sure
of
collagen
to
collagenolytic enzymes.
Extra-
polating
from work on dental caries
[51],
an
increase
in
proton
concentration
will
result
in the
partial
demineralization of
hydroxyapatite,
because
it will
buffer
the
changes
in
pH
at its own
expense.
Microbial fermentation of
bone
proteins by
anaerobic
pathways
could lead to the total loss
of
the
organic
fraction of bone since the
products
of
the reaction
perpetuate
the
reaction;
total
loss
of
the
organic
fraction, however,
is
not
likely.
As the
rate
of anaerobic
decomposition
slows due to the
lack of
metabolites,
oxygen
will
diffuse into the
sys-
tem. Eventually, the rate of anaerobic degradation
will be
surpassed
by
the rate
of
oxygen
diffusion
and
the
system
will return to its
aerobic
state,
when
the rate
of
aerobic
degradation
will
be determined
by
the
concentration
of
bio-available
organic
mat-
ter
[52].
Catalyzing
bone
decomposition
To
decompose
bone,
a
microorganism
must be
able
to
obtain
energy
from the
collagen
and mineral.
For the microbial
enzymes
to
gain
access to the
col-
lagen,
the microbe must also
be able to
demineral-
ize the
bone,
or
grow
in
an environment
where
demineralization occurs
(e.g.
a
low-pH soil).
Enzymes
Enzymes
are
proteins
which
can increase
the rate
of
(catalyze)
biological
reactions between
106-
and 108-
fold. As well as
increasing
rate,
enzymes
are
specific
in the
reactions which
they
will
affect.
An individ-
ual
enzyme
will
catalyze
a
specific
reaction with a
unique
substrate
or
group
of substrates.
Enzymes
that
disrupt
proteins
are called
proteolytic enzymes
or
proteases,
and
enzymes
that are
unique
in
their
ability
to
hydrolyze efficiently
the
triple-helical
regions
of
collagen
under
physiological
conditions
(i.e.,
moderate
temperature
and around neutral
pH)
are called
collagenases. Collagenases
are
complexes
of several different enzymes, each of which has a
different
catalytic
function.
There are two
accepted
types
of
collagenase [53].
Collagen degradation by
vertebrate
collagenases
Vertebrate
collagenases
(tissue collagenases)
disrupt
unmineralized
collagen
into
only
two
fragments by
action at a
specific
site within the
al(I)-chain,
a sin-
gle
glycine-isoleucine
bond between residues 772
and 773
[54].
The
enzyme appears,
therefore,
to rec-
ognize
the whole
collagen
molecule
configuration.
Collagen degradation by
microbial
collagenases
On the other hand, microbial collagenases recognize
small
amino acid
sequences.
All
microbial
collage-
nases examined so
far
appear
to have
the
same
amino
acid
sequence requirements
for
cleavage
[55-59];
hence examination of the action of a
well-
characterized bacterial
collagenase
can be included
here.
The anaerobic
bacterium Clostridium
histolyticum
produces
a
collagenase
complex
of
six
enzymes.
All
are
highly
active
against
collagen
and
devoid
of
other
proteolytic
activities.
Study
of their amino
acid
sequence requirements
for
cleavage
is
challeng-
ing,
since
purification
of
these
enzymes
is
difficult;
however, the requirement for one of them (,3-colla-
genase)
has been demonstrated
[60].
Unlike verte-
brate
collagenases, 3-collagenase
does not have
a
rigid sequence requirement,
but will
cleave
between
the
X- and
the
glycine-
residues in
any
of the
sequences
below:
-glycine-Y-X-glycine-proline-hydroxyproline-
-glycine-Y-X-glycine-alanine-arginine-
-glycine-Y-X-glycine-Z-alanine-
where
X-,
Y-
and Z- can be
any
of
the amino
acids
which constitute
collagen, except glycine.
Microbial
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Microbial
taphonomy of archaeological
bone
collagenases,
therefore,
have
active sites
along
the
length
of
the
collagen
molecule which
are
dictated
by
amino acid
sequence
rather than whole
molecule
configuration.
Like
tissue
collagenases,
they
are
metalloproteinases
containing
a
zinc ion at the
active site
[61, 62].
Microbial
collagenases
cleave the
collagen
helix
into
a
range
of
short
peptides
by hydrolysis
at
mul-
tiple
sites
along
the
triple
helix.
The
major
product
following
treatment
of
Type
I
collagen
with the
col-
lagenase
complex
from
Cl.
histolyticum
is the
tripeptide
glycine-proline-hydroxyproline, although
many
other
products
are
generated.
Like vertebrate
collagenases,
microbial
collagenases require
that the
collagen triple-helix
be
demineralized
before the
enzyme
can
gain
access
[63].
Collagen
degradation
by proteases
Microorganisms
that
produce
collagenase may
vary
in the rate at
which
they
will
decompose
the
bone.
The
microbial
by-products
of
metabolism and
the
presence
of
other
enzymes (e.g.
proteases)
can
also
affect
the
collagen.
Proteases
appear
to have no
action
on
the
collagen
triple-helix;
it could be
argued
that their
only
value in
collagen
decomposi-
tion is
that
of
reducing
the
short
peptides
released
by
collagenase
action to
single
amino acids.
It
was
suggested
above
(see
'Collagen degradation
by
microbial
collagenases')
that the
only enzyme
sys-
tem
capable
of
cleaving
the chains
of
Type
I
colla-
gen
in their
helical
regions
is
the
collagenase
system. This
may
not be the case.
One
protease, chymotrypsin (enzyme
classifica-
tion number: E.C.
3.4.21.1),
has been shown to
have
collagenolytic
activity.
Classically,
chy-
motrypsin
should
have
little effect
upon
collagen,
since
peptide
bonds
which
involve
hydroxyproline
are resistant to its action
[10].
Chymotrypsins
from
the
mid-gut
of
shrimps
(Penaeus
monodon,
P.
japon-
icus
and
P.
penicillatus)
have been
shown
to
have
some
collagenolytic activity [64].
The
shrimp chy-
motrypsins
are resistant to the
standard
a-chy-
motrypsin
inhibitors,
and some have been shown
to
have a
higher
affinity
for
collagenolytic
activity
than for other proteolytic activities [65].
Collagenolysis
by non-specific
proteases
has been
promoted by
low
pH
[66].
Pepsin
(E.C.
3.4.23.1)
in
acetic
acid
is
the standard
laboratory
method
by
which
Type
I
collagen
is
removed
from demineral-
ized
bone
[67].
This
enzyme
is
used to cleave
the
covalent
bonds
holding
the
triple-helix together.
Unlike
collagenase,
it
has no action
upon
the
helices themselves.
Indeed,
low
pH
could be the
mechanism
by
which
some
fungi produce
'tunnels'
(see 'Diagenetic changes'
below)
within
archaeologi-
cal
bone
[68].
Although
no
microbial
proteases
capable
of
cleaving collagen
in
its helical
parts
have
yet
been
described,
the
possibility
of this
decomposition
pathway
cannot be ruled out.
The taphonomyof bone
Taphonomy
was defined above as the
study
of
all
changes
which occur within
an animal
after
death
[3].
The
taphonomy
of bone is influenced
by
the
physical
and chemical
characteristics
of
the sur-
rounding
environment
and
the destruction
of the
surrounding
soft tissue. There are two
main
processes by
which
bones and soft
tissue become
degraded,
both of which affect the
stability
of the
associated
collagen.
These
processes
are
enzymatic
(which
includes
both
autolysis
and
microbial
decomposition)
and
chemical;
both are
affected
by
temperature.
Limitations
of
burial
temperature
The
range
of soil
temperatures
is dictated
by
the
air
temperature
and the soil
depth.
In
Britain,
at
a
depth
of
300cm,
the
temperature
range
is 10.5
?
2?C
[69].
Published
studies
of the
action
and char-
acteristics of microbial
collagenase
have been car-
ried out
at
28?C
and
37?C. The
microorganisms
that will
produce collagenases
at soil
burial
temper-
atures
cannot
be
extrapolated
from this
literature,
since
a
significant temperature
reduction of 18-
27?C will severely restrict many different species,
including
Clostridium
histolyticum [70].
Microbial
studies at low
temperatures
are
required.
Although only
a few
studies of this
nature have been
undertaken,
results
so far
indicate
that certain
types
of
bacteria
and
fungi
can
be
iso-
lated
repeatedly.
The bacteria
and
fungi
able to
produce collagenases
at low
temperatures
are
pre-
sent
in
archaeological
bone and
associated
soils
in
very
low numbers
when
compared
to the
total
microbial
population.
The
bacteria
and
fungi
are
obligate
aerobes,
able to
grow
over
a
wide
range
of
temperatures (4-39?C)
and
pH
values
(3-6-9-0)
[68,
71]. The bacterial species isolated (Pseudomonas,
Aeromonas,
Xanthomonas)
produce
metabolites
which are
toxic to
fungi
and therefore
can
compete
successfully
with a wide
range
of
fungal
species
(see
'Microbial interactions'
below).
Autolytic changes
As a
cell
dies,
it
releases a
mixture
of
enzymes
from
the
lysosomes.
These
enzymes
have an
autolytic
(self-destructive)
function
and
usually
take the form
of
proteinases
and
DNAses,
which
speed up
the
destruction of the
tissue and
its
component
cells.
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A.M. Child
Autolysis usually
follows
very rapidly
after
death;
even
in
the
short
interval
between death and
burial,
the
osteocytes,
marrow and
neuro-vascular
bundles
undergo
autolysis
[72]. Autolysis
is
self-limiting
and,
after a certain
stage
is
reached,
the
cells
remain stable for long periods of time [73]. The
majority
of
changes
in
bone, however,
affect the
extracellular matrix
proteins
(i.e.,
collagen)
which
are not amenable to
autolysis.
Microbial
changes
Augmenting
the
processes
of
autolysis
is microbial
decomposition:
autolysis
opens up
the
soft
tissues,
thus
increasing
access for
microorganisms.
Decomposition
of whole
bodies involves the loss
of
both soft and hard
tissues,
and both
aerobic
and
anaerobic environments
will
be
achieved within the
rotting
flesh.
Due to the
presence
and
high
numbers of
gut
flora
(which
include some
microorganisms
capable
of
inducing
dental caries
[74]),
the bones
within the
abdomen
and thorax
will suffer the
demineralizing
effects
of
putrefaction
for
longer
than the
long
bones
or the skull. This is
borne out
in
some
stud-
ies,
but not
in
others
[75,
76]. Laboratory
studies
using
bones
inoculated
with
microorganisms
[77]
support
the
premise
that
soft tissue destruction
aug-
ments hard tissue
loss.
Biostratinomic
changes
Autolytic
and
microbial
changes
appear
very
soon
after death. Autolytic destruction can occur within
10
seconds
following
death of
the
cell
[73].
The
types
and
degree
of microbial
destruction
will be
dictated
by
the environment
in which
the
corpse
lies.
If burial does not
immediately
follow
death,
the
growth
of
microorganisms
which would
nor-
mally
be
prohibited
by
the low burial
temperatures
will
be
promoted
(e.g.
Cl.
histolyticum).
Once the
body
has
cooled,
these
microorganisms
are
unlikely
to
grow,
but it
is
possible
that the
temperature
of
the
decaying
body
may
increase
sufficiently
to
allow
for their
growth.
It
is
probable
that Cl.
histolyticum
has its most
important role in the breakdown of collagen in the
pre-burial
stage. Collagen
breakdown
will
occur as
the
bones and associated
tissues
lie on
(or slightly
below)
the surface
of the soil.
Cl.
histolyticum
is
present
in the
soil,
but also
in
the
gut
of humans
and
some animals
as normal flora.
Diagenetic changes
Janaway
[41]
considered that
soil was
less
impor-
tant
in the
initial
stages
of
decomposition, arguing
that the
body
will
create
its own
environment
which
in turn
will
modify
the effects
of the
surrounding
soil.
Studies
in
soil
microbiology
have
shown that
this
is not
likely.
Microorganisms
are
introduced
into
farming
soils so that certain
growth
character-
istics of the
soil
may
be
improved.
These micro-
organisms
have been
genetically manipulated
to
give required
characteristics.
In
almost all
cases,
these introduced microorganisms die out; they do
so as
a
result
of
competition
with
the
normal
soil
flora,
although
some success has been achieved
by
genetically manipulating
soil isolates
and
re-intro-
ducing
them into the same
environment
[78].
If a substrate
(i.e.,
a
corpse)
which contains
microflora
is
added to
soil,
its own microflora
will
be
destroyed by competitive
interactions
with the
normal soil flora.
This
may
take
only
a few
months
or
years,
but the
microorganisms
present
within
the
corpse
at death
may
induce
diagenetic changes
before
the
indigenous
population
is
destroyed.
Overall,
the initial
taphonomic changes
induced
in
a corpse may be the result of autolytic mechanisms
and inherent microbes.
The most
significant diage-
netic
changes
seen
in
a
corpse
are more
likely
to be
due
to the action of
soil macro- and microflora.
A
particular type
of
diagenetic change
is that
seen
in
microscopical
focal destruction
(MFD).
These are
localized 'tunnels'
thought
to
be
pro-
duced
in
bone tissue
by
the action
of
microorgan-
isms
(for
a
review,
see Bell
[79]).
The dimensions
of
the
MFD
are identical
with the dimensions
of
microorganisms;
the
microbial metabolites
cannot
diffuse
far into the
dense bone tissue.
In some
types
of
MFD,
mineral
redeposition
along
the
interior
walls of the 'tunnels' has been noted. It is thought
that this is
due to the death of
the
microorganisms:
when a
microorganism
dies,
the
pH
of the
sur-
rounding
medium rises
due to the release of
ammo-
nia and
other microbial
metabolites.
This rise
in
pH
will
promote
the
re-precipitation
of dissolved
hydroxyapatite.
An
unexpected
alteration
of bone
protein by
the
bacterium
Pseudomonas
fluorescens
has been
shown
[77]. Decomposition
studies
using
various
strains of
this
bacterium,
both
singly
and
in
concert,
has
shown
that the bacterium
has
the
facility
to
change
the rate
of racemization
of the
aspartic
acid
residues in the insoluble collagen of bone.
Post-excavation
Microbial communities
are
affected
by
environmen-
tal disturbances.
The inherent
microbial
population
within
archaeological
bone
probably
receives
its
greatest
disturbance
on excavation.
The
problems
created
by
the sudden
alteration
of redox
potential
will
be
exacerbated
by storage
in
a
warm
'finds
tent'.
The microbial
loading
within
the bone
will
already
be
significant;
alteration
of
temperature
alone will increase
microbial
growth
rates
since,
generally,
enzyme
reaction
rates are doubled
for
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Microbial
aphonomy
f
archaeological
one
every
10?C rise in
temperature
[80].
The
con-
comitant
ncrease
n
oxygen
concentrationwill
pro-
mote
rapid
aerobic
decomposition
of
organic
components.
Fast-growing
ungi, previously
held
in
check
by
burial
conditions,
tend to
flourish at the
expenseof other organisms.With the presenceof
metabolites
rom
fungal
action,
the
rate
of
decom-
position
of the
bone
will,
to a certain
extent,
be
controlled
by
the interactionof the inherent
micro-
bial
species
(see
'Microbial interactions'
below)
until
physical
conditions
(e.g.
storage
at
controlled
relative
humidity)perform
his
function.
Chemical
hydrolysis
If
the mineral
phase
of bone retains its
integrity,
then
collagen
can
only
be lost
following
chemical
alteration.
A
number of chemical transformations
will occur and will continueafter
death,
such
as the
processof non-enzymiccrosslinking,but the most
significant hange
will
be
hydrolysis
of
the
peptide
bond.
A
simple,
conceptual
model
of
collagen
peptide
bone
hydrolysis
has
been
suggested.
This model still
requires
much work before
it can
be
usefully
applied
to mineralized
ollagen,
but
it
fits
well with
many
observed
phenomena
81].
The rate of colla-
gen
loss from the
bone will
depend
upon
the rate of
peptide
bond
hydrolysis,
the
rate of
diffusion of
these small
fragments
out of the
bone
and
the
rate
of
post-mortem rosslinking.
Crosslinkswill form as
a
result
of the
continued
non-enzymic process. 'Vegetabletannates' in the
burial environment
will
bond to
the
collagen
[82].
The
degree
of
bonding
by
these
tannates
will
depend upon
the
rate of diffusion
of
these chemi-
cals into the bone. This diffusion
will be
enhanced
following
demineralization f
the bone.
It
is
likely
that
the
presence
of these
compounds
n the
bone
will
physically
inhibit
the
action
of
collagenolytic
enzymes.
Limitations
of microbial
decomposition
Once microbialdecompositions stopped,the only
degradation process
occurring
is chemical. The
causes of the
reduction
n
microbial
activitymay
be
multifactorial. f
any
one or a combinationof these
conditions is
met,
then microbial
decomposition
may
slow
or
even
stop,
but chemical
hydrolysis
will
continue.
Burial
temperature
As
the
rate of
decomposition
of
the soft tissue
slows,
due to
its
removal
by
aerobic
and anaerobic
decomposition,
he
temperature
f
the
decomposing
matrix will fall.
The
fall
in
temperature
will
slow
microbial
activity.
This
slowing
will
have a
positive
effect on the fall in
temperature,
ntil
the
tempera-
ture of
the
decomposing
material
reaches that
of
the
surrounding
oil.
Alkaline and acid
soils
Alkaline
soils
will
buffer
the microbial
acids and
inhibit
the dissolution of the
bone mineral.
Conversely,
acidic soils will
tend
to
promote
bone
decomposition,
although
this is
only
a
generaliza-
tion.
The rate of
hydrolysis
of
peptide
bonds
is
increasedn both acid and alkaline
environments.
Microbial interactions
Many
bacteria and
fungi generate by-products
of
metabolism that
are
antagonistic
to other
micro-
organisms i.e., antibiotics). These chemicalshave
a
suppressant
ffect
both on membersof the same
genus
and on
completely
different
genera
83,
84].
Generally,
competition
between
microorganisms
tends to
prolong
the
life of the substrate.
The
greater
he
variety
of
microorganisms
within
a
sub-
strate,
the
longer
it is
likely
to
survive,
since
some
microbial
energy
must be directed owardscontrol-
ling
other
microorganisms
rather than substrate
digestion
alone.
Non-microbial
inhibitory
substances
Burial
environments
may
inhibit
the
growth
of
microorganisms apable of degradingbone. The
presence
of
copper(I)-but
probably
not
iron(II)-
ions
as well
as
other
inhibitory
substances
(e.g.
vegetable
tannates)
may
promote
the survival
of
both
the
soft and
the hard
tissues
[85].
Extremes
of temperature
Extremesof
temperature
an
promote preservation
of both the soft and the hard tissues:
they
are
known to survive
n
desertsand
permafrost
egions
[37].
Desiccation
will
reduce microbial
activity
and
hence the
only
mechanism or
collagendegradation
is chemical hydrolysis,the rate of which would
depend
upon temperature.
Enclosed
environments
Enclosed environmentswhere there
is
little
or no
leaching
will
promote
the
preservation
f
bone.
An
equilibrium
will be reached
between
the
microbial
products
of metabolism and
the
bone mineral
buffering
capacity.
The
presence
of
the microbial
metabolites
will inhibit
further microbial
growth,
since
they
are toxic to the
microorganisms,
and
thus
the
microbial
populations
will
slowly
decline.
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A.M. Child
Conclusion
The various
pathways
for the
microbial
taphonomy
of
archaeological
(and
historical)
bone have been
defined here
and,
even
though
an exhaustive list has
not been
given,
it can be seen that
a
bewildering
range
of reactions is
possible.
These include dem-
ineralization of the
bone,
damage
due to
the
action
of
microbial
enzymes
(both
collagenases
and
pro-
teases),
the microbial
production
of MFD
(micro-
scopical
focal
destruction)
and the alteration
of
the
proteins
following
decomposition.
Acknowledgements
The author
would like
to thank Professor R.D.
Gillard,
Dr
Matthew
Collins,
Dave
Watkinson,
Susan
Hardman and
Naomi Earl-Turner for their
helpful comments during the preparation of this
manuscript.
Thanks are
also due
to
Dr
J.
Morgan
and
the
staff of the Cardiff
Royal Infirmary,
Bacteriology
Department,
for
their
kind
permission
to use
the
laboratory
facilities for the microbial
iso-
lation work.
The
project
was funded
by
the Science
&
Engineering
Research Council
(Science-Based
Archaeology
Committee).
References
1
BUNN,
M.
K.,
'Saran as a treatment for archaeo-
logical
bone',
undergraduate
dissertation,
Cardiff (1987).
2
HUECK,
H.
J.,
'The biodeterioration of
materi-
als-an
appraisal'
in
The
Biodeterioration
of
Materials,
ed.
A. H.
WALTERS nd
J. J.
ELPHICK,
lsevier,
London
(1968)
6-12.
3
EFREMOV,
.
A.,
'Taphonomy,
a new
branch of
paleontology',
Pan-American
Geologist
74
(1940)
81-93.
4
TRIFFITT,
.
T.,
'The
organic
matrix of bone' in
Fundamental and Clinical Bone
Physiology,
ed. M. R.
URIST,
Lippincott, Philadelphia/
Toronto
(1980).
5
GREEN,
M., ISAAC,
D.
H.,
and
JENKINS,
G.
M.,
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relationship
with
collagen'
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Author
ANGELA
M.
CHILD
studied
microbiology
at the
University
of London and
worked for several
years
within the
National
Health Service. She
went
on
to
study archaeological
conservation at the
University
of Wales
College
of
Cardiff,
graduating
in
1988.
Her
special
interest was the
decomposition
of
organic
materials and she
completed
her PhD
on
aspects
of bone
decomposition
in
1992,
followed
by
a
two-year
SERC
(SBAC)
post-doctoral fellowship
which continued the
investigation
of
the interaction
of
microbial
populations
in
the
decomposition
of
archaeological
bone.
She is
currently
working
in
the
field of ancient
biomolecules,
on the interaction
of
osteocalcin with hydroxyapatite. Address: Fossil
Fuels & Environmental
Geochemistry,
NRG,
Drummond
Building, University of
Newcastle,
Newcastle
upon
Tyne
NE1
7RU,
UK.
Resum--La
taphonomie
est
l'etude
de tout
changement qui
intervient sur un animal ou sur
-une
plante
apres
sa
mort. Les os
sont les
principaux
materiaux
d'origine
animale
d
survivre
dans
l'environnement
archeologique.
C'est une source
importante
d'informations
sur
les
relations,
les
regimes,
les
maladies et les
dges
des
peuples
(et
des
animaux)
des anciennes
cultures. Pour trouver et
interpreter
ces
informations,
il est
besoin
de
conser-
vateurs
et
d'hommes
de sciences
archeologues qui
connaissent les
processus
de
changements
taphonomiquesqui
peuvent
advenir
aux os. Ces
changements
sont nombreux:
ce
papier
tente de
definir quelques-uns
de ces
princi-
paux
changements, qui peuvent
etre
attribues a l'action
variee
des
microorganismes.
Zusammenfassung-Taphonomie
bezeichnet das Studium aller
Veranderungen
an Lebewesen und
Pflanzen
nach
dem
Tod.
Knochen sind das
vorherrschendeMaterial lebenden
Ursprunges,
das sich im
archaologischen
Rahmen erhalt. Sie
sind die
Quelle fir
eine
Vielzahl
von
Informationen
uiber
Beziehungen, Nahrung,
Krankheiten und
Alter von Menschen
und Tieren
vergangener
Kulturen. Damit
diese
Informationen
gesammelt
und
interpretiert
werden
k6nnen,
miissen Konservatoren
und
archdologische
Wissenschaftler
ein
Bewujftsein
ur
taphonomische
Veranderungen
entwickeln,
die sich
in
Knochenmaterial
abspielen
konnen.
Die
vorliegende
Arbeit
versucht,
wichtigste
in
Knochen
feststellbare
Veranderungen
zu
definieren,
welche den
zahlreichen
Aktivitdten
von
Mikroorganismen
zuzuschreibensind.
Resumen-Tafonomia
es el estudio de todos los cambios
efectuados
en
las
sustdncias animales
y vegetales
despues
de la muerte
de
las mismas.
De los restos de
origen
animal,
el
hueso
es el
principal
material
per-
Studies in Conservation40 (1995) 19-30 29
8/17/2019 Microbial taphnomy of archaeological bone
13/13
A.M.
Child
durable dentro
del dmbito
arqueol6gico.
El hueso es una abundante
uente
de
informacion
acerca de las
rela-
ciones
sociales,
dietas,
enfermedades y
edades
de
gentes
(y
animales)
de culturas
pasadas.
Para
extraer
e
interpretar
esta
informacion,
es necesario
que
los conservadores
y
cientificos
arqueol6gicos
esten conscientes
de
los
procesos
de
cambio
tafonomicos
que
pueden
ocurir
en el
hueso. Estos
procesos
de cambio son numerosisi-
mos.
Este
trabajo
propone
la
definicion
de
algunos
de los
principales
cambios observados
en hueso
y
atribuibles
a las acciones varias
de los
microorganismos.
Studies in Conservation40 (1995) 19-300
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