<<

are

1.0

mature

berries

with

berry

.

ribbed

hypothesis

indicated

hybridization

minus),

following

Cloning

the

aggregates

Abstract

Hector

Group

macroscopic

Introduction

bacterial

the

may

The

mussels

berry.

and

II

The

Castro,

mussels

sulfate

in

and

the

Report:

be

phylogenetic

the

focus

subsequent

that

found

goal

sequencing

presence

derived

The

supported

salt

(

reducing

mussels

(1

Yoshiko

strongly

of

of

in slime

-

marsh

Berries

our

4

the

selected

present

from

mm

incubation of

research

present

groups:

are

matrix

the

,

Fujita,

of

may

green

suggested

diam.)

)

involved

16S

presence

in

shallow

ingest

that

the

sulfur study

Katie

rDNA

was

purple

purple

in

produced and

berries

contributes

that

the

the

were

the

in

of

was

pools

bacteria.

Patterson,

cytophaga.

extracted

the

the

inlet

these

or

sulfur

bacterial

“berries”

to

observed

and

pink

formation

in

sulfate-reducing

by

investigate

or

molluscs

the

to

bacteria

1

the

to

Field

pond

aggregates

and

from

determine

components

the

Sippewisset

from

Enrichments

.

expelling

Erik

is

observations

aggregation

of

the

(most

play

the

necessary

the

the

Zinser

berries

Sippewisset

found

The

berries,

how

berries

a

bacteria

closely

berry-like

role

of

Salt

Group

and

results

and/or

the

suggested

lying

for

of

in

in

Marsh.

or

whole macroscopic

berries,

the

and

the related

the

the

II

berry

of

on

why

Salt

pink

bacterial

Microbial

initial

salt

development

cytophagas,

laboratory

cell

and

We

the

precursors.

Marsh.

but

they

to

marsh

material.

fluorescent

in

aimed

formation

presence

Thiorhodococcus

reject

purple

the

species are

Diversity

led

The

July

simulations

top

formed.

and

to

them

of

The

to

or

Atlantic

identify

of

layer

berries

in

a 27,

of

the

also

in

pink

the

the

as

the

situ

1998 1998

presence

the

checkerboard

length

cytophaga,

least

Cloning

of phototrophs

(Banin,

using

the

unsuccessful;

slime.

observed

phototrophs,

berries.

characterization,

In

2.

answer

1. of

rod-shaped

berries

order

1997

How

What

the

an

polymorphism

Attempts

Previous

1997).

following and

of

the

approach

Seitz

Microbial

to

/why

many

bacterial

was

and

purple

address

and

following

sequencing

hybridization.

embedded

bacteria

the

within

et

highly

are

“symbionts”.

Using

small

sulfate

al.

to

students

microscopy,

authors

sulfur

phylogenetic

including the

species

Diversity

disintegrate

these

(1993)

(RFLP), selected

conserved.

rod-shaped

berries

berries

and

questions:

reducing

in

of

bacteria

questions

speculated

in

a

are

16S

reported

RFLP

the

slime

enrichment

Banin

as

Course,

formed?

shallow

DGGE

field

present

rDNA

the

inoculum,

groups: Microbial

bacteria.

and

bacteria,

The

matrix

and

in

slime

an

observations

also

that

that

cytophaga.

(denaturing

Banin

the

checkerboard

extracted

pools

in

approach

DGGE

compared cultivation,

the

the

it

purple

slime

with

which

Diversity

he

Scanning along

was

dominant

in

again

berries?

successfully

proteolytic

analyses

2

the

around

composed

from

encompassing

appeared

sulfur

with

and

gradient

investigated

marsh.

different

hybridization

microscopy,

Course

electron

laboratory

the

some

species

bacteria,

the

indicated

berries

to

enzymes

of

enriched

The

gel

coccoid

spirochetes

berries

have

stabilize

complex

microscopy

in

electrophoresis),

the enrichment

Group

goals

sulfate

simulations

suggested

the

and

that

attempted

results

composition

purple

using and

for

berries

of

molecular

the

the

II

polysaccharides.

both

reducing

glucoronidases

and our

Microbial

confirmed

aggregate.

restriction

confirmed

species

sulfur

cultivation,

the

research

were

diatoms,

to

was

purple

characterize

presence

and

of

techniques

bacteria.

bacteria,

developed.

purple

composition

the

sulfur

Diversity

the

fragment

the

were

They

July

within

berries,

molecular

were

During

of

presence

sulfur

27,

to

also

at

the

the

1998 1998 of

and

enrichment

in

and

bacteria,

between

Seitz

2.0

references

Section

to

berries

applied following

1.1

major

employed.

laboratory

as

three

the

for

apply

obtain

Enrichments

Organization

et

berries

iron

role

Microscopic

other

and

al.

The

5. to

This

individual

the

additional

pure

sections.

the

(1993),

are

experiments:

Section

in

experiments

reducers.

from

purple

The

various

types

year

are

the

berries.

listed

cultures

results

the

described.

formation

our

Banin

berries

of

sulfur

6

of

characterization

techniques

analysis

Section

in

berry-derived

includes

enrichments,

No

the

group

Section

Section

of

of

to

(1997),

for

growth

phototrophs,

Report

our

these

simulate

from

of

2

The

sought

heat-tolerant

and

our

contains

investigations

the

7.

3

applied

three

the

presents

and

characterizations

was

field

conclusions

berries.

enrichments.

using

to

possible

same

techniques.

our

observed

kinds

confirm

observations

and

a

to

summary

group

the

the

respiratory

the

and

the

of

conditions

media

suggest

molecular

investigation

different

and

cytophagas.

bacteria.

the

3

in

suggested

In

In

the

of

recommendations

findings

of

provided

and

Section

addition,

that

the

and

heat-tolerant

the

ponds.

leading

laboratory

characterization

In

1

results

mussels

fermenting

that

6S

of

addition,

of

We

4

for

rRNA

more

the

the

the

several

Group

These

to

therefore

from

the

microscopic

berries

previous

in

berry

and simulations

field

clones

Microbial

the

we

for

bacteria;

II

are

the

bacteria

used

formation

salt

observations

future

data

Microbial

are

attempted

the

various

investigators,

from

marsh

described

sulfate

berries

generated

techniques

for

are

Diversity

are

research.

the

enrichments

cyanobacteria;

conserved

presented

were

may

Diversity

to

berries

reducing

July

as

and

enrich

in

inocula

from

play

course

as

Finally,

the

27,

applied

by

well

in

a

the

1998 1998

phase

some

first

flasks

made

The

incubation.

enrichments

temperature primary

thiaminium

nicotinic

mi/I

NH4C1,

bicarbonate

84

with

microscope

2.1

below.

enrichments,

g/l

was

ethanol

of

Sulfate

rings

dark

either

of

with

stock

Both

the

Berries

the

enrichment

a

20.0

acid,

discrete

cocci,

of

H2/C02

vitamin

ethanol

ethanol

These

secondary

of

dichioride,

for

Na2HCO3,

buffered

the

slide.

were

Reducing

growth

g/l

and

sulfate

5

were

5

ethanol

mg

NaCI,

and

days,

performed

brown

primary they

Crushed

stock:

(20

secondary

headspace,

bottles

Ca-

were

phase

washed

minimal

reducing

but

3.0 are

and

mM)

and

Bacteria

and

D(+)-pantothenate,

2

colony,

100

observed) not

mIll

enrichments

not

g/l

bright

were

5

then

berries

H2/C02

at

and

in

mg

the ml

MgCl*6HO,

and medium

discussed

bacteria.

respectively.

Na2S,

30

sterile

finally

incubated

cyanocobalamine.

Na2SO4

consisting H20,

H2/C02

cocci,

°C.

the

were

consisting

enrichments

H2/C02

1X

(pH

4

moved

were

which

then

further.

The

mg

concentration

(20

enrichment

initally

7.1-7.3)

of

15

Two

subcultured 4-aminobenzoic

second

added

0.5

mM)

4

motile

could

to

primary

mg

of

(80%)

The

30°C

g/l

showed

3

colony

at

pyridoxamine

cell

or

consisted

to

Due

KC1,

was

be

>30

curved

other

H2/C02 several

showed

a

enrichments

of

interpreted

types:

for

bicarbonate

to

into

a

types

°C

0.15

turbidity

trace

hazy,

four

problems

final

rods,

for

secondary

acid,

of:

times

Group

long

turbidity.

g/l

grew

and

element

enrichment

one

undefined

incubation.

dihydrochioride,

0.2

CaC12*2H20,

consistent

1

within

as

thin

Na2SO4

and

into

buffered

day,

mg

in

II

with

g/l

the

both

rods

liquid

then Microbial

solution

D

Hungate

KH2PO4,

Agar

then

3

the

the

(+)

colony

stages

types

enrichments.

(20

that

with

All

crushed

minimal

first

incubator,

moved

enrichments.

shakes -Biotin,

mM).

SL1O,

subsequent

twitched,

tubes

the 30

are

in

week

10

Diversity

(in

0.25

July

the

mill

mg

with

described

to

were

which

medium

10

The

and

and

room

g/l

of

the

27,

of

mg

The

a

flat

1

an

1998 1998

weeks.

temperature

(0.05%

berries

spread

2.3

noted

agar

pairs,

purple

Erik

2.2

performed.

(TEM)

cycle

Cytophagas

Purple

surfaces.

Zinser’s

by

and

onto

of

were

Enrichments

sulfur

Table

tryptone,

The

analyses

a

cytophaga:

the

positive

two

under

protocol

crushed

Sulfur

Fluorescence

phototrophs

independent

1

likely

In

contains

types

0.05%

of

addition,

oxic

hybridization

these

Phototrophs

for

predominant

with

vegetative

and

of

conditions.

cytophagas

yeast

data

plates:

results

isolates

a

present

project

in

we

microscope

for

situ

extract

enriched

rods,

YPG

of

several

with

hybridization

PSB,

are

report.

in

the

Many

were

the

in

microcysts

described

(yeast

the

purple

which

slide

for

berry,

of

performed

The

different

green

the

a

water

extract

putative

and

is sulfur

key

5

a

isolates.

()

in

sulfur a

motile

and

passed

(70%)).

large

section

results

colony

+

on

bacteria

spores.

green-sulfur

peptone

FISH

and

dilute

bacteria

coccus

through

obtained

4.

types

Incubations

transmission

probe

(PSB)

complex

Secondary

+

Group

that

with

arose

glucose

a

bacterium

hypodermic

are

(see

forms

enrichments

irregular

II

over

that

were

media

sect.

electron

Microbial

in

and

tight

there

the

sea

perfomed

4).

from

plates.

ovoid

course

aggregates

water)

needle,

are

are

microscopy

the

Diversity

described

at

cells

July

shakes

Washed

of

and

berry,

at

least

and

two

room

27,

often

TYE

on

then

two

were

as

1998 1998

in in

cytophaga

hybridization

None

motile

J

I

H

G F

E

D

C

B

A

Isolate

of

in

the

liquid,

species

isolates

with

TYE

TYE

TYE

YPG

YPG

YPG

YPG

YPG

YPG

YPG Medium

and

from

the

displayed

gliding

flavo

the

Table

berry

FISH

motility

pale

spreading

opaque,

agar pale border

degrader

rough

yellow

yellow

rough,

yellow

round,

very

large

mucoid

all

large

irridescent

round

opaque

rough

translucent

Char.

Colony

1.

with

of

probe

yellow

pink,

degrader

Isolates

mucoid

opaque

opaque

the

translucent

on

pale

dark

center,

these

off-white

common

surfaces.

morph.

(see

agar

from

enrichments.

section

6

Cytophaga

characteristics

Nor

of

length,

thin

rods

curved,

motile

length

rods

4).

cocci

cocci,

phase-bright

diplo-bacilli

cocci,

cocci,

in

irregular

Char.

Cell

did

gliding

chains

Hence

rods

of

the

(?)

some

rods

some

some

no

clumps

var.

Enrichments.

clusters

motile

chains

chains

of

one

in

rods

evid.

Group

we

of

var.

candidate

cytophagas:

were

of

II

10+

unable

Microbial

(J)

thin

show

to

isolate

Diversity

rods,

July

a

positive

non

a

27,

1998 1998

re-cultivate

had

that

insufficient

possible

darkening

enrichment

substances

for

ferrihydrite,

(approximately

and

enrichment

Several

of

one

electron

40

reducing

identical

Pfennig

2.4

the

been

humic

mM

sulfur

40

week

Iron

bottles,

In

mM

that

days

Seven

ferrihydrite

inadvertently

bottles

donor

the

to

was agent

of

substances,

a

Reducing

iron can

in

were

was

ferrihydrite;

slight

that

the

and

the

secondary

later

the

limiting;

and

washed

in

and

reducing

30

and

inoculum,

containing

iron

subcultured

described

used

10

secondary

turn

darkening

the

a

ml

carbon

mM

sulfate

ferrozine

[amorphous

solids

Bacteria

which

as headspace

solids

chemically

omitted

berries

a

enrichments,

2,6-anthroquinone

inocula, (ii)

activity

few

which

for

source.

was

in

non-reduced

enrichments.

40

in

into

may

of

weeks

the

assay

the

were

from

the

mM the

not

Fe(OH) 3 1

in

from

3

and

was

enrichment

serve

reduce

sulfate

other

different

orange

The

a

added

crushed

the indicated

ferrihydrite

into

60

very

the

primarily

the

as

medium

bottles

ml

bottle

anoxic

the ferric

bottles

reducing

berries.

Another

electron

as

little

iron

as

disulfonate

stoppered

types

on

incubation

an

with

the

the

7

also

iron.

were

solids,

a

activity

supernatant sea

electron

with

were

formulation.

slide

electron

presence

of

AQDS,

bacteria,

possible

acceptors

began

water

incubated

secondary

Five

a

bottle);

again

indicating

and

headspace

(AQDS).

was

it

acceptor.

medium.

was

ml

to

acceptor,

observed

the

of

reason

except

rather

incubated

observed,

darken.

in

aliquots

ferrous

and

No

recognized

material

Group

without

.

enrichments:

reduction,

AQDS

further

of

(iii)

than

for

Instead

that

The

and

after

80/20

iron

The

from

II

at

the 5

except

was

headspace

the

no

Reduced

mM

10

medium

30

Microbial

is

attempts

one

earlier

in

that

lack

sulfide

the

H 2 /C0 2

iron

mM

the

a

was

divided

°C.

the

model

acetate,

for

week.

(i)

a

medium

of

primary

solids,

acetate

medium.

sulfur observed

5

positive

humic

composition

a

growth

was

at

were

mM

slight

Diversity

between

compound

30

It

July

40

added

source

was

is

contained

acetate

as

°C.

made

mM

was

primary

27,

in

After

one

two

as

1998

1998

to was

conducted

pairs

the

16S

3.3

hybridization.

labelled

(position

Two

3.2

DNA

beadbeater

with

Microbial

from

slides,

3.1

3.0

TA

rDNA

Cloning

PCR

segment.

DNA

set

Molecular

ethanol.

the

system

Amplified

cloning

PCR

and

Berries

with

of

1492)

different

using

reaction

sequences

Diversity

extraction

primers

passed

in

reactions

and

digoxigenin

(Promega)

In

the

Further

kit

PCR

for

were

the

the

characterization

sequencing

bacterial

presence

(Invitrogen).

samples

several

amplification

were

program

cases

course

products

in

washed

were

analysis

the

employed:

was

(DIG)

where

times

1

of

were

Genbank

conducted

guide

6S

RNA1

used

with

were

a

rDNA

of

mix

Ten

and

through

PCR

extracted

of

(1998).

the

filtered

to

sized

bacterial

(Bruce

(1)

of

clones

universal

purify

database

sequences

amplication

from

according

phenolichloroformlisoamyl

universal

syringe

by

sterilized

The

using

Paster,

were

the

the

electrophoresis

16S

using

reverse

8 method

berries

DNA.

was

the

needles

to

sent

forward

rDNA

personal

was

the

seawater,

DNA

BLAST.

conducted

for

(position

was

not

is

Microbial

and

with

based

automatic

(position

lysis

achieved,

cloned

comunication).

on

(2)

crushed

Phylogenetic

a

Group

an

protocol

on

by series

1492)

universal

Diversity

agarose

into

cell

alcohol,

comparing

8)

sequencing

the

II

and

of

for

between

Escherichia

lysis

described

Wizard

Microbial

smaller

checkerboard

forward

universal

gel.

and

course

analysis

through

them

two

of

later

PCR

gauges.

a

(position

in

guide

Diversity

coli

microscope

reverse

to

500

was

July

the

precipitation

the

preparation

existing

use

base

using

(1998).

27,

DNA

8)

of

1998

1998 a

aggregates

the

(Figure probes

sequenced

extracted

brown

incubation

bacteria

(SRB)

analysis PCR

and

membrane

3.4

berries

very

310

oligotroph

Odontella

Thiorhodococcus

presence

pink

Checkerboard

base

products

similar

hybridized “berries”

enrichment,

In

3),

Checkerboard

(Banin

Of

(PSB)

(Figure

flocs

from

the

pairs).

in

formed

the

with

sinensis

according

the

1095,

of

1997,

(one

first

signal

amplified

(from

a

SRB,

enrichment,

ten

1997;

the

(mussel

mussel

2).

The

cytophaga

CH

with

base

by

minus

clones

hybridized

PSB

(4)

For

(91%

Hybridization

for

spirochetes,

non-berry

a

Figure

to

clone

(Figure

hybridization

all

mussel

pair

five

crushed

the

the

the

enrichment

with

(94%

sent

the

similarity),

(2)

difference

pond

protocol

pond

similar

second

1).

(100%

the

samples.

2),

or

only

for

incubated

mixed

ponds

similarity),

by

pseudofeces),

the

and

berries,

DIG

berry

sequencing,

with

passing

to

CH

was

similar

(see

given

(CH)

universal

flavobacteria.

culture

in

and

T.

out

forward

(lane

The

the

the

the

conducted

minuss

with

section

(5)

of

two

in

following

two

through

for

DNA

probe

Sippewisset

five 500)

35)

of

the

PSB

six

probes,

clones

primer

9

the

(7)

clones

PSB

clustered

5.2;

was

Microbial

berry-like

clones

to

from

for

pink

first

(1:10

using

a

The

a

DNA

and

lower

were

syringe

samples

the

from

clone

the

were

one

19

sand

Salt

DNA

dil.)

were

cytophaga,

a

SRB

with

FlavofBacteroides

base

related

dilution

minislotfblot

Diversity

than

one

and

aggregates

related

previously

(1:10

Marsh)

was

(Figures

were

most

extracted Group

purple

species,

pairs

pond

five

in

positive

to

dilution),

the

to

used:

1:10

closely

berries.

(3)

were

a

and

berry,

course

II

sulfur

the

3).

freshwater

first

from

from

sequenced

sulfate

from

and

Microbial

apparatus

88%

(1)

chioroplast

for used

CH,

related

five

bacteria

the

guide

and

the

probe

1:100),

In

purple

the

gamma-

similar

reducing

in

the

mussel

berry

pond

but

(8)

berry-like

obligate

the

from

using

(1998).

to

Diversity

and

second

sulfur

DNA

July

(6)

revealed

and

of

first

for

berries,

and

SRB

the

five

a

bacteria

it

27,

the

nylon

CH

The

CH

was

last

1998 1998

phosphotungstic

Caulobacter-

slides,

4.2

contrast

surrounding

coccoid

was

aqueous

polysaccharide

aqueous

were

4.1 4.0

hybridize

we

for

(lanes

aipha-,

Transmission

believe

the

examined

Crystal Microscopy

smeared

and

grids

Berries

37

In

PSB

and

images

solution

solution

to

order

with

suspended

these

coated rod-shaped

them.

40).

berry

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like

on

under

were

capsules

any

from

to

acid

of

of

bacteria

a

The

visualize dii.

Electron

Figure

slide

with

copper

Staining

washed

of

bright

(PTA;

the

in

probes

SRBs,

1:100,

the

bacteria

sterile

plastic

and

(Gerhardt

berry.

to

4

DNA

violet

sulfate.

field

pH

includes the

in

(Figure

be

Microscopy

stained

spirochetes,

the

for

seawater

filtered

7).

important

and

matrix

stained

oil

samples

brown

the

for

et

TEM

carbon.

After

immersion

6a),

using

berry

the

2

al.,

sterile

minutes.

surrounding

berry,

(80%).

dark

and

crystal

1994).

showed

from

partial

(TEM) and

components

the

PSB

TEM

a

purple,

seawater

flavobacteria

Anthony

10

long

the

the

(1000X)

and

violet-stained

The

The

drying,

The

the

pink

samples

berries.

curved

the

the

berry

with

presence

air-dried

dye

of

(80%),

purple

sand

staining

berry

microscopy.

a

the

was

a

cover

suspension

were

flagellated

This

light

(lane

dii.

berry

cytophaga

washed

crushed

berries,

film

sulfur

of

Group

method

result

heavy

slip

1:10,

purple

bacterial

36).

microbiota.

was

was

bacteria,

II

The

was

off

rod

and

along No

between

was

metal

covered

capsule

for

Microbial

clones

put

with

results

(Figure

staining

the

aggregates

prepared

unexpected,

bacterial

with

on

stained

crushed

mussel

a

two

9

layer

the

with

20%

were

and

other

6b).

revealed

Diversity

slide

microscope

for

July

with

a

dil.

(wlv)

(Figure

10

berries

obtained

phase

TEM 1%

TEM

because

did

and

27,

1:10

1%

(wlv)

not

1998

1998

it

on 5),

fluorescence probe

Na 2 SO 4

from

sulfur

FITC

GSulf

Cy3 Flavo

Rhodamine

SRB2 Dye

Probe

The

NaCl,

samples modifications.

and

from

isolates

4.3

Figure

was

then

following

Fluorescent

the

also

the

(Figures

bacteria

Name!

rather

Probing

7

Whole

enrichments

to

berry

were

crushed

shows

1998

applied

detect

throughout

than

fixed

was

(see

Green

8c

probes

sulfate-reducers

CFB

Phylogen.

Microbial

cell

of

Berry

one

sulfate-reducing

to

and

with

In

0.5

the

more

Figures

fluorescent

in

division

samples

of

with

Sulfur Situ

M.

8d),

berry

were

samples

4%

a

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the

microscope

informative.

Diversity

Group:

either

All

but

paraformaldehyde

Hybridization

morphotypes

8a

used:

cell

was

from

samples

no

and

were

in

ethanol

as

complicated

autofluorescence

situ

bacteria,

the

8b;

noted

course

prepared

slide

5’-cttttargggatttcctctg

5’

5’-tcagtrccagtgtggggg

Sequence:

hybridization

SRB

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-cgygcgccrctytact

or

observed,

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before

signal).

handout

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H 2 !C0 2

enrichments

cytophagas,

counterstained

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by

for

by

the

11

red

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washing

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passage

putative

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without

a

showed

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color,

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autofluorescence

hours.

short

followed,

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performed

(ethanol

through

several

while

slightly

SRB

with

the

good

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green

probing

Group

probe.

DAPI

some isolates

wash

hybridization

as

times

a

with

curved

sulfur

54

57

58

Tm

on

hypodermic

electron

of

of

II

cells

buffer

Most

the

(blue

the

in

(

from the the

Microbial

bacteria.

C)

rod.

sterile

berry

following

showed

predominant

enrichments!isolates

cells

signal

donor)

contained

Hyb!Wash

the

with

needle.

and

sea

showed

anaerobic

37

37

37

The

in

Diversity

partial

with

the

several

July

water

all

protocol

0.9

SRB2

All

figures).

Temp

berries.

purple

27,

or

(80%),

M

berry

no

1998 1998

the

Temperature

9).

through pond

assess

5.1

5.0

analysis. the

showed

control

berry

cells

phototroph

The

fluorescence,

lab

A

Field Field

TYE

FISH

and

from

site

with

the

with

The

The

(a

which

no

enrichment

do

Observations

Observations

characterization

known

this

results

the

detectable

berry

collected

enrichment

Gsulf

not

and

which

water

Flavo

culture

form

salinity

pond

cytophaga)

support

probe

flows

and probe

may

samples.

in

at

signal.

would

and

from

other

and

the

showed

were

the

indicate

the

of

in

provided

the

pond

hazy

Laboratory

the

the

and

showed

show

conclusion

Hence,

ponds

measured

environment

The

berry

berry.

a

out

and

brown

differences

positive

a

results

in

no

positive

from

positive

a

to

pond,

the

strong

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evidence

attempt

in

colony

that

Simulations

of the

salt

the

hybridization

the

surrounding

the

these

signal. we

identification

positive

in

12

adjacent

field;

marsh.

culture

inlet,

to

from

the

have

that

understand

measurements

amount

pH,

these

the

Probing

and

isolated

was

signal,

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tidal

the

with

anaerobic

the

impure,

berry

were

of

pond

channel

of

both

channel

some

the Group

these

why

an

target

and cytophagas.

pond

SRB

were

are putative

the

it

the

sulfate-reducer

of

two

as

sulfide

makes

II

presented

1

was

yellow

the

is 6S

berries from

the

observed

Microbial

isolates

connected

rRNA

cells

cytophagas

conducted.

tide

sense

were

the

While

swarmer

form

changes from

in

berry.

within

awaits

in

measured

that

Table

Diversity

enrichments

to order

in

July

the

a

an

the

not

from

cells

the

further

(Figure

positive

2.

27,

inlet

to

berry

all

cells.

in

the

from

1998 1998

Berries

bacteria,

berry

berries

indigestible

it

are

hypothesis

simply

we bacteria

organisms material present

demissa).

Channel Inlet

Pond

is

not

devised

possible

are

found

The

therefore

consume

digested

The

The

in

the

(Langdon

present

(Figure

While

the

which

suggests

second

two

first

or

berry

inlet

that

in

berry

unpalatable

27

31-33

31

Temp.

Table

the

hypotheses

by

hypothesis

the

accumulate in

berry

10). the

feeding

feed

would

and

hypothesis

the

the

berry

pond

that

berries

ribbed

2.

Atlantic

on

(°C)

mussels,

formation

water

Newell,

the

form

Site

pond.

into

,

itself.

to

mussel

as states

addressing

berries

in

that

the

Characterization

the

states

in

they

—6

—6

—6 pH

ribbed

the

1990).

but

This

Mussels

the

mussels.

serves

the

berry

that

inlet

feed.

is

form

are

that

mussel,

mussels

hypothesis

a

mussels,

the

the

common

pond

rather

After

where

to

mussels

independently

,

in

This

mussels

potential

protect

the

and

is

02

10-12

filter. 10-13

13-14

observing

regurgitated.

scenario

the

Data

13

like

inhabited

inlet

suggests

inhabitant

the

(mg/i)

form

mussels

its

do

all

role for

In

berry

were

bacterial

not

bivalve

the

dissolved

this

further

the

of

mussels

that

by

contribute

that

observed

berries

would

the

reside,

Berry

scenario,

of

If

0.01-0.08

0.2

Atlantic 0.5-1.5

S 2

mussels

the the

this

mussels

molluscs,

components

Group

suggests

(mg/i)

excreting

organic

be

Pond.

bacterial

salt

or

and

hypothesis

expelling

to

excreted

a

mussels

ribbed

play

II

marsh,

precursor

when

berry

and

that

are

Microbial

matter,

in

berry-like

components

that

by

20

30

30

Salinity

mussels

suspension-feeding

the

the

formation.

berry

the

by

would

berry-like

is

making

the

berry

tide

supported,

to

the

,

mussels

formation.

the

mussels

Diversity

(%)

mussel.

ingest

comes

July

(Geukensia

aggregates,

aggregates

them

“mature”

of

pink

This

are 27,

and

the

the

then

in

not

1998 1998

collected from

pond

water

chamber

chamber

the

were

5.2

pseudofeces.

berry

berries,

production.

rejected

(Bayne

intriguing

berries

components

berry berries

excreted

are

formation

washed

Laboratory

the

established

that

collected

may

pond.

A

The

together

in

and

but

tidal

as

containing

containing

from

by

did

series

the

because

in

pseudofeces.

reject

Newell,

hypothesis

into

the

This

of

The

fact

not

channel.

of

berry

The

the

from

the

of

mussel

the

(Seitz

the

with

Simulations

contain

be

second

mucus

them

berry

slime

laboratory

it

berries.

pond.

water

water

berries.

berry

the

the

1983).

is

two

et

Treatment

known

that

as

are

pond

mussel

berry

matrix

serves

hypothesis

berries.

As

al.,

collected

collected

pond.

replicates pseudofeces.

Maturation

not

the

The

pseudofeces

Glass

1993)

experiments

and

pond,

that

yet

berries,

that

to

mucus

mussels

This

Treatment

4

aggregate

bowls

“mature”--meaning

a

is

from

from

contributes

consisted

per

also

sediment

portion

produced

hypothesis

of

that

or

treatment.

This

allows

the

the

in

the

were

are

berry

were

contributes

collected

the

the

3

of

berry

berry

berry

produced,

theory

of

from

consisted

14 used

material

salt

in

to

conducted

precursors,

for

particles

two

allows

the the

pond

may

pond.

Treatment

marsh

the

the

as

suggests

berries

from

mussel

aggregation

experimental

that

to

nearby

possibility

occur

molluscs

ingested

of and

for

that

pseudofeces

Treatment

may

the

to

a

they

are

the

in

sediment

mussel

determine

that

and

are

after

nearby

Group

pond,

1

a

ingest

formed

possibility

consisted

lack

chamber

by

increase

being

not

the

of

that

the

filter-feeding

in

2

chambers.

and

the

components

by

II

berries

pond.

the

collected

production.

consisted

berries

the

a

in

rejected

if

Microbial

bacterial one

chamber

pink

components

the

containing

mussels

their

of

slime

that

Treatment

a of

are

mussels

are

sand

mussel

mucus the

the

from

Five

as

of

that

mussel

present

deposited

containing

species

molluscs

contribute

pseudofeces

Diversity

berries

a

bacterial

collected

July

mussel

holds

water

treatments

a

is

in

of

nearby

4

a

the

27,

was

in

in

the

is

in

the

in

the

1998

1998

to

the a

strongly

6.0

digested

rapidly

berries

looser

excreted

mussels

(PSB)

berries

can

presence

treatment

Treatments

ensure

incubated

consisted two

designed

Conclusions

likely

berries

and

and

The

from

To

that

(Seitz

(<

Mussels

suggest

were

by

the

of

to

4

of

be

1

for

less

further

green

results

the

the

did

pink

or

day)

1,

determine

PSB

the

a

attributed

et

fed

three

2,

chamber

(2)

discrete

mussel mussels

not

berry al.,

that

in

4,

sulfur

filtered

sand

and

berry

and

the

of

Treatment

and

increase

weeks

1993).

the

the

the

formation

Recommendations

pond

the

is

but

if

bacteria

clumps,

pond

to

5

filled

had

mussels

essential

field

and

the

GSB did

abilty

the

in

rather

and

sufficient

in

treatment

the

water

excreted

not

with

presence

3

observations

in

size.

excreted

but

(GSB).

the

of

of

laboratory.

play

result

were

the

to

water

mussels

additional

spiked

they

berries

berry

The

form

an

food

the

excreted

conditions

of

in

As

were

berries

essential

collected

results

purple

the

PSB

formation

for

with

of

produced

to

to

and

the

Pond

aggregates.

formation

berries.

filter.

produce

clearly

Future

15

and

mussels

enrichment

the

as

during

of

sulfur

would

role

unwanted

from

water

the

GSB,

laboratory

in

by

aggregated

Research

Treatment

in

berries

simulation

bacteria,

the the

filtered

of

the

mussels

facilitate

was

the

suggesting

The

berries.

mussel.

process

cultures

berry

material

formation

changed

under

simulations

Group

aggregates

the

the

in

bacteria.

5

pond.

experiments

(1)

treatment

of

served

The

spiked

The

of

dominant

controlled

that

II

or

an

suspension

every

both

of

two

pseudofeces.

Microbial

color

Treatments

increase

these

differed

the

with

as

pond

The

purple

berries

few

the

3

berries.

of

component

bacteria

suggest

in

conditions,

the mussels

water,

control

the

days

feeding.

in

that

from

sulfur

Diversity

mussels

incubated

size

July

were

pink

they

in

Therefore,

that

they

were

the

very

and

of

order

bacteria

27,

sand

of

were

the

the

the

not

1998

1998

in to

relationship

dark

in

the

berries

berries

using

disaggregation

1998).

texture.

using

of

berries

in

laboratory

the

simulations.

sulfide-rich

berry

the

PSB’s

second

purple

most

molecular

microbial

We

Autoinducer

in

together,

Future

Another

excreted

Berries

maturation

in the

should

observed

probable

hypothesis

berry

between

the

dark

purple

research

of

collected

dark

possible

composition by

in

techniques,

exhibited

the

be

did

order

the

via

activity

number

that

berry

purple

compared

sulfur

berries.

not

concerning

mussels

should

the

topic

to

from

while

result

color

addition

sulfur

phototroph

determine

berries

was

whether

(MPN)

as

This

the

of

further

the

to

are

compared

in

and

detected

future

granules.

berry

determine

the

berry

PSB

may

lacked

not

of

phototroph

enumeration.

berries

pursue

mussels

an

other

medium,

yet

research

of

pond

necessitate

disaggregation.

appropriate

in

sulfur

to

light

“mature”

It

the

bacteria

excreted

if

the

this

and

will

was

16

they

pink

berries

composition

the

is

pond

granules.

autoinducer

berries

be

Application

the

supported

the

are

purple

and

berries

to

disaggregation

by

of

berries,

population

characterization

(Pat

the

indeed

interest

the

that

produced

In

sulfur

aggregates.

Fidopiastis

were

mussels

within

incubation

by

addition,

activity.

Group

although

the

of

to

the

bacteria

full

MPN

distribution

same.

more

by

the

technique. results

are

II

of

the

after

personal

berry.

of

It

they

enumeration

Microbial

in

extensively

sulfur

fully

It

should

mussels

from

the

the

of

is

a

differ

possible

developed

mucus

within

the

6-day

berry

granules,

an

Incubation

project

be

laboratory

originally in Diversity

in

July

determined,

incubation

study

pond

the

the

will

holding

shape

that

report,

most

berries,

in

27,

require

results

the

the

of

terms

and

1998

1998

the of Group II Microbial Diversity 1998 July 27, 1998

Other suspension-feeding organisms in the salt marsh may also produce berries. Future studies should address the role that these organisms play in berry formation.

Finally, additional enrichment conditions for cytophagas should be conducted. For example, cultivation on TYE and YPG plates under oxic and anoxic conditions and at different temperatures could be tried.

17 Group II Microbial Diversity 1998 July 27, 1998 7.0 References

Banin, U. 1997. Identification of the bacteria forming the “berries” purple macroscopic aggregates in Great Sippewissett Salt Marsh. Microbial Diversity, Marine Bioloogical Laboratory, Woods Hole, MA.

Bayne, B. L. and R. C. Newell. 1983. Physiological energetics of marine molluscs. In: Saleuddin, A. S. M. and K. M. Wilbur (eds.). The , Physiology, Part 1. Academic Press, New York, 4: 407-5 15.

Gerhardt, P., R. G. B. Murray, W. A. Wood, and N. R. Krieg. 1994. Methods for General and Molecular Bacteriology. American Society for Microbiology, Washington, D. C., p. 35. Langdon, C. J. and R. I. E. Newell. 1990. Utilization of detritus and bacteria as food sources by two bivalve suspension-feeders, the virginica and the mussel . Marine Ecology Progess Series 58: 299-310.

Seitz, A. P., T. H. Nielsen, and I. Overmann. 1993. Physiology of purple sulfur bacteria forming macroscopic aggregates in Great Sippewissett Salt Marsh, Massachusetts. FEMS Microbiology Ecology 12: 225-236.

18 (% Difference)

I I

Purple sulfur sp. WHO1 (1998)

Purple Sulfur sp. Clone C 13 (1997) Thiorhodococcus minus

Rhabdochroma tium marinum roseopersicina Chromatium okenii

Thiocystis ge/a tinosa

Chroma tium vinosum

Escherióhia co/i She wanella putrefaciens

FI&OP 1

Notes:

• •

Dental

Sediment Pink Berry

(Bacteroides

Squid

Cytophaga

All

(see

flock

SRB

All

All Flavo/Bacteroides

samples

samples

Cytophaga

V. Cytophaga

Enterics

Universal

Blank

plaque

Blank

Bruce

Actinomyces

All

gazogenes

All

Rothia

Universal

All

probes

Cyanos

Methylotrophs

sp.

samples

S.

Strept.

has

identified

SRB

Streptococcus

Veillonella

oralis

from

and

samples

for

sp.

have

SRB’s

have

‘S

2

1

sanguis

Checkerboard beriy

-a

related

berry

berry

explanation)

gave

sp.

specific

flavobacteria

last

(but

have

no

bacteria)

a year

not

signal—probably

,_

different

SRB

*

Plaque

the

(last

øø.*

identified

and

specific

year

samples

hybridization

.1-rn

distributions

1

sample

not

p

species

last

all

DIG

berries

may

year

primers

found of

.,

a)..D

have

and

streptococci

a)

had

of

a)

cj.

a)

in

flavobacteria,

methylotrophs

were

both

environmental

the

c

berry)

not

Cytophaga

and

used.

and

other

but

(arrow--

flavobacteria

not

species)

Plaque

samples

Staff

bacteria,

samples

the

0

0

hard

specific

including

Sediment

Samples

to

see)

species

flavobacteria

June29,

of

I 1998 Checkerboardhybridization 7/24/9 8

13579111315171921232527293133353739

S — a Berry“PurpleSulfur” - ft. ft ft Betas-all Nitrosolobus/Nitrosovibrio Nitrosomonasspp R.: 0 EntericsI some gammas p. ft S Methylotrophicbacteria ANGAlteromonassp. ) __•. Alphas-all ANGShewanella sp. Vibrio gazogenes Berry “Plastid’ SRB2, some deltas SRB, some deltas BerrySRB clones C16/C18 LoGCGram Positive Green Sulfur-all Planctomyces-all a Spirochetes Flavos-all Bacteroides Cytophaga berry ClO Cytophaga berry C9 Cyanobacteria Microcoleussp. Lyngbiasp. Nostocsp. Oscillatoriasp. Phormidiumectocarpi. Synechococcus sp. ————S ._ 545. Universal 135 79111315171921232527293133353739

Key:

1. Silvana-salt pond I 12. Milvaenrich t2+ 02 23. Karin Cyan. Pure 34. /FeYoshiko-H 2. Silvana-salt pond 2 13. Milvaenrich t4+ 02 24. Scott- Begg. Environ 35. Pond Berry 3. John oyster 14. Milvaenrich 02 25. Andreas Deep Sea 36. 2Pksand berry 1/10 t8+ 4. Group I- ED 15. Milva enrichment t6 w/o 0 26. Andreas Deep Sea 37. Pksand berry 1/100 5. Group l--LD 16. Grp IIsediment 27. Andreas [no good) 38. Brown berry 6. Group I-MD 17. Grp IIsediment [No good) 28. Andreas Deep Sea 39. Pink sand 1/10 7. Group 1-GI [No good]] 18. [No good] 29. Yoshiko ThioS 40 Mussel 1/10 8. Group I-P2 19. Patti Sip. Hi Nitrogen plot 30. /FeYoshiko-H Group I-G3 20. Patti Sip. Low Nitrogen plot 31. Grpll--PSB ‘ Group l-B4 21. Patti Sip. Control plot 32. 2Grp IICyto/PS 11. +0Milvaenricht 22. Karin Cyan. Assoc. 33. Gm IISRB 02 FL&URE ‘ 0 C

-‘1

c:z

-t FiGuPE 5 -n Q > rn c5 V 0 1

• • • • ••• • . • •

I FIGURE

10