A Survey of Microbial Diversity

11 Pages·1996·17.5 MB·

by  Diana Lipscomb

A SURVEY OF MICROBIAL
Diana Lipscomb
DIVERSITY^
Abstract
The development of new technologies increasing our understanding of prokaryotic and eukaryolic microbial di-
is
New
was
versity in terms of abundance, diversity, and ecological function. studies reveal greater diversity than previously
known and have highlighted the importance of these organisms in ecosystem function. There no consensus on the
is
new
phylogenetic relationships of the various unicellular organisms at the phylum and kingdom level, and, as long as
Some
taxa and characters are discovered, innovations in classifications of the kingdoms will likely continue. general
conclusions are already clear. First, is obvious that classifications that divide organisms into just two, three, four, or
it
five kingdoms are too simplistic. In all of these simple schemes, one or more of the kingdoms ultimately contains a
heterogeneous group of diverse taxa and either paraphyletic or polyphyletic. Alternatively, a multi-kingdom system
is
some
provides a more realistic view of the diversity of life. Concomitant with this is the realization that traditional
An
categories such as monera, algae, protozoa, or fungi can no longer be considered distinct phylogenetic groups.
many
overall scheme of classification that reflects our growing databases will hardly look like those followed in text-
books, but more accurately the relationships of the unicellular microorganisms.
will reflect
it
Today, most people are aware of the economic sediment, or soil, and are in symbiotic association
and ecological importance of multicellular animals, with multicellular organisms. Information about the
plants, and fungi. But this appreciation does not size and nature of microbial populations is very in-
and
usually extend to the importance of biological di- complete because of difficulties in detecting
versity of microorganisms. Possibly this is due to extracting them from the environment. Neverlhe-
the scale at which most microorganisms live. The less, by piecing together various sources of infor-
and
majority are too small observe with the naked mation (and taking into account that activity
to
eye. Many are able to move and constantly change biomass measurements can be artifacts of the meth-
position and so cannot be easily tracked. They have ods used) we are beginning to understand microbial
short lives ranging from a few hours to a few days, diversity in terms of abundance, diversity, genetic
but they can also form protective cysts and remain variability, and ecological function.
environment an
in the in inactive slate for years.
Microorganisms can respond rapidly changing ABUNDANCE
to
becoming
conditions in their environment, active
J
may show marked
Microbial populations
^ differ-
^
and1 growi.ng, or i• nact.i• ve and1 encystt ed wi-tfhU-in mi•n- ^ ^
distances (McAlice, 1970;
^"^'^^ "^^"^ ^^^7 ^"lall
makes them more
utes or a few hours. All of this
&
Krumbein. Ashby Rhodes-Roberts, 1976)
1971;
many
study and people
difficult for scientists to for
few minutes
i" '"'^^^^^ ^^ort as a
°^ ^^^'^"g^ ^«
and understand. Nevertheless, aware-
to relate to
&
during environmental (Erkenbrecher Steven-
flux
ness of microbial diversity important both be-
is
many
Even
J J v son, 1*9^75). taking this into account, in
cause 1humans depend on mi•crobes f many eco- '^^ 6 ' J
tor
'
-'
environments numbers of microbial cells are high
and
logical services (production of oxygen, mineral
^or example, Fenchel recently estimated
(1992)
nutrient cycling, etc.) and because some forms are
r that a one-centimeter core of coastal marine sedi-
agents oif dise.a.s^e^. T» :. ftih,e^ p1^u,.r*.p*.ose^ o^tf ftUh;i^s p^.a.p..e.r^ ft^o
11 is
X
u menl contained 4 10'" bacterial cells, 10* het-
try to convey somet.h1 i• ng about* t*uhe dJ*iversi•t* y otf t^uhe '
erotrophic flagellates and amoebae, 10« chlorophyll
microbial world: what known and what uncer-
is is
and 2000
"-containing microorganisms,
ciliates.
tain, and the prospects and challenges for survey-
ing microbial diversity.
DIVERSITY
Scope of Microbial Diversity
made
Microbial communities can also be up of
many Many
Microorganisms include both prokaryotes and different species. eukaryotic microor-
unicellular eukaryotes (the protists). They are ubiq- ganisms can be identified by a taxonomic expert
uitous and in great abundance in all natural water, using standard microscopical methods (e.g., Fois-
Support from U.S. National Science Foundation grant (DEB-9305925) gratefully acknowledged.
is
^
^ Department of Biological Sciences, George Washington University, Washington D.C. 20052, U.S.A.
Ann. Missouri Bot. Gard. 551-56L 1996
83:
Annals
of the
Garden
Missouri Botanical
Using and
sner, 1991). silver stains light micros- revealed evidence for a previously unrecognized
example,
copy, for Finlay et al. (1993) studied the photosynthetic bacterium and a unique heterotro-
kinds (phylum
of ciliated protists Ciliophora) in- phic bacterial group.
habiting the sandy sediment of a Spanish stream. An alternative molecular approach involves clon-
They sampled cDNA
this stream on just one day in winter ing transcribed from 16S rRNA using a
(water temperature was 4°C at the warmest time of primer complementary conserved
the universally
to
day). They marked out square meter, and took rKNA &
1 region of (Ward et a!., 1992; \^eller Ward,
from 13 random sediment samples by pushing
it a 1989). Ward (1990) used method study
et al. this to
cm
3-cm-diameter tube 3 into the sand, capping
it, the thermophilic (-50°C) microbial community
and extracting the sand. From small amount of
this from Octopus Spring in Yellowstone National Park,
sand, they identified 65 species of ciliates belong-
Although community had been
this previously stud-
ing to 50 genera, from 17 orders. Considering the
by more methods and was
ied traditional believed
broad
diversity of ciliate habitats available within
^o be relatively simple (Ward et 1987), the anal-
al.,
the area, the importance of physical transport pro- cDNA
y^j, the revealed eight (hstinctive bacte-
^,f
cesses in the river basin, and the fact that many
lal groups that did not match sequences known for
ciliatt* species have a cosmopolitan distribution,
it
'ultured species including those previously isolated
probable
that the species richness they recorded
is
snrinirs
i^^^
fj.^^^^^
is representative of the sandy sediment of the river
Since these studies, such molecular methods
first
m
wmter.
have facilitated our exploration of the free-living
Analysis of the diversity of prokanotic microor- r %
r
/ uivcrsity oi maruie an(ii es*tuar• me wat.ers /
•' irr mm (e.g.,
. r
ganisms more 1 1because
^ is 11^dif1ficult they often lack o inoo\
r\
bchi midjt. * i 1991; DeLtong, 1992), organisms
et al.,
enough 1 •
morphological complexity b, e accurately
to
(Amann
colonizing solid surfaces et al., 1992), or-
identified using microscopic methods. Traditionally,
ganisms in water treatment activated sludge (Wag-
culturing techniques were used recover prokar-
to
ner and organisms
et al.. 1993), in soil (Torsvik et
yotes from environment and characterize
tlie to
1990; Masters 1991; Stackebrandt
al., et al., et al.,
them
by and
their physiological nutriticmal require-
1993). These methods have also been used de-
to
ments. Because none of these culturing methods
scribe microorganisms living in association with
permit and
the isolation characterization of pro-
all
otlu^r organisms, such as the chemoautotrophic bac-
karyote species, microbiologists attempted obtain
to
teria symbiotic in invertebrates living near hydro-
meaningful diversity data from the use of a wide
thermal vents (Slahl et al., 1984; Distel et al.,
range of techniques, each of which permits the
1988), the cellulolytic nitrogen-fixing symbiotic
study of a small fraction of the marine biomass
total
inoQ D innox bacteria that enable shipworms (wood-borine mol-
f\ .• 6
(Auslin, 1988: But»t. on et^ al1., 1993). TE?ven so, onl1 y i v
"'^ principal source of food
^^'^''^ ^^
*^ "^'"'''^ ^
a small percentage of the prokarjotes that actually
^^^^^^ prokaiyotic symbionts of
^^ ^^^^
^\-
exist in a habitat are revealed by these methods
^^^f*^^
(Embley
& various protists et al., 1992; Springer et
(Brock, 1987; Staley Konopka, 1985).
Embley
1^^^' et 1993), the bioluminescent
al.,
More recently, modern molecular genetic tech- ^*-'
&
symbionts (Haygood
bacterial of fish Distel,
niques have enabled more
mic-robiologists detect
to
1993), and the cellulolytic symbionts in the rumen
microbial taxa (Stahl et al., 1989; Bull et al, 1992;
mammalian
Embley & Amann of herbivores (Angert et al, 1993), and
Stackebrandt, 1994;
et
al.,
identify both plant and animal pathogens
1995). These molecular tools allow microbiologists ^^ (e.g..
to extract and analyze nucleic acid sequences (pri- Relinan et al, 1990; Gundersen et al, 1994).
rRNA Caution must be used in interpreting results be-
marily sequen(res) directly from the environ-
new
^^^^^ the molecular methods can be problem-
ment, thus circumventing need
the culture pro-
to
The ^^ic. In addition to technical problems, such as
karyotes before identifying them. studies
first
characterizing prokaryotes directly from environ- pr^be sensitivity in certain conditions, it can be
sequences organisms
mental samples used sequences difficult to retrieve of rare
of electrophoreti-
(Amann PCR
rRNA
cally separate<l 5S molecules et al, 1995). Furthermore, probing of
(Stahl et al.,
DNA
1984; lane 1985; These mixed samples can suggest the presence of
et al, Stahl et al. 1985).
rRNA
techniques were refined for 16S (Olsen etal, nonexisting organisms by forming chimeric se-
1986) and made easier perform with the advent quences assembled from sequences of different
to
of polymerase chain reaction (PCR) technology. species (Liesack al, 1991). Nevertheless,
et
is
it
This modified approach was used by, for example, obvious that molecular techniques provide extreme-
Giovannoni al
et (1990) to characterize the diver- ly useful tools for analysis of microbial diversity
&
sity of bacterioplankton in the Sargasso Sea and (Stahl Kane, 1992).
553
Number Lipscomb
Volume 4
83,
1996 Microbial Diversity
SYSTEMATIC DIVERSITY
ECOLOGICAL FUNCTION
As more being learned about microbial diver-
is
and
Microorganisms diverse ecological roles,
fill
becoming commonly used clas-
clear that
it is
^^^y,
key environmental processes are
practically
all
&
Whit-
schemes Jahn Jahn, 1949;
sification (e.g.,
Microorganisms
are
driven by microbial diversity.
&
1969, 1977; Margulis Schwartz 1988) are
taker,
essential biological nutrient cycling, sulfur oxi-
to
descnb-
oversimplified and simply inadequate for
methanoge-
and ammonification,
dation reduction,
and mul-
ing the true nature of the diversity, that
and methane Symbiosis with mi-
oxidation.
nesis,
kingdoms needed (Leedale, 1974; Taylor,
are
t^pl^
many
major by which
croorganisms a. route
..............
i.s. -1
/
Woese
.^ n .^ 1_9_78'; Lipscomb, 1985, 1989, 1991; et al.,
mult, icellul1 ar euk1 aryotes 1have gained access to ^^ _/
-j vr
V
1990). Certainly t.,he c,hanges andi rapid prolifera-
complex metabolic (Douglas, 1994).
activities
new schemes microorgan-
of
tion of classification
These include nitrogen fixation, production of es-
an
J isms are confusing to many, but they represent
• 1 ami•no acid1s and vi•*tami•ns, cel11lul1 ose jd^engr*r.ao- '^"''' '^^^ &
sential
m l
. r
.
period microbi iali research from
invigorating
and photosynthesis. Microorganisms are es-
dation,
which a new, and hope ul more realistic and sta-
A
lie*- breakdown ly
major food webs. of the
sential to all
emerge,
system of microbial classification will
^^ ble,
annual carbon fixation and1 oxygen prod}u,.crt.ri.ro.n^ kb,y. ^^"^' ""J ^
an individual photosynthetic microbe group is not
PROKARYOTE SYSTEMATIC DIVERSITY
much
available. has been estimated that up to as
It
80%
open ocean con-
as of the production of the is animals, and even eukary-
j^ contrast to plants,
tributed by photosynthetic protists (Piatt et al., microorganisms, the morphology of prokar>'olic
^^[^
&
Andersen,
Takahashi Beinfang, 1983;
1983; simple serve
microorganisms in general, too to
is,
&
and
1992), and in lakes chrysophytes (protists) cy- (Olsen Woese, 1993;
^s a basis for classification
40%
up primary
anobacteria contribute to of the Amann 1995). Classification traditionally de-
et al.,
productivity (Konopka, 1983). pended on by culturing followed by char-
isolation
In ecosystems that lack direct photosynthetic in- organisms according physiological and
acterizing to
put, microorganisms are even more important as biochemical However, much of our under-
traits.
primary producers. Chemoautotrophic bacteria in prokaryote phylogeny quite recent,
standing of
is
environments such as deep sea vents and marine jy^ largely to the recent advent of modem molec-
assem-
sediments provide energy support a rich Sequences from
to sequencing methods.
genetic
^i^j.
blage of heterotrophic microbes and animals (Jan- RNA, example, have revealed two
ribosomal
for
&
nasch Taylor, 1984; Cavanaugh, 1994). groups prokaryotes. This distinctiveness
distinct of
enormous otrophic new
caused Woese et al. (1990) to propose a su-
microbes, continual grazing by heterotrophs keeps perkingdom category, the domain, and to create
Some
their numbers in check. of the biomass pro- three domains: Archaea (for the archebacteria),
duced by photo- and chemo-autolrophic microor- and Eucarya the eukaryotes). Despite
Bacteria, (for
ganisms is consumed directly by animals (e.g., the criticism of this system (e.g., Cavalier-Smith, 1993),
0-40%
widespread use
1 today.
in
is
it
carbon from bacteria; Moriarty et al., 1985), but the Archaea and Bacteria are both prokaryotic, but
majority consumed by heterotrophic microorgan- the archebacteria have no peptidoglycan in their
is
membrane composed
isms either from pools of dissolved organics, or as cell wall, have lipids of
decomposers and primary consumers (Pomeroy, branched carbon chains attached glycerol by es-
to
1974; Williams, 1981; Fenchel, 1982, 1986, 1987; Hnkage, use methione as the start signal for pro-
ter
rRNA
Azam et 1983; Ducklow, 1983; Hagstrom, tein synthesis, lack the loop that binds ri-
al.,
and
1984). These heterotrophs include prokaryotes, bosomal protein in the eubacteria, lack the
(Azam common arm sequence (guanine-thymine-pseu-
protists, and their protistan predators et al..
tRNA
1984 found
douridine-cystine-guanine) of the in
(phylum and
Ciliophora) eukaryotes eubacteria.
Sherr, 1988). Ciliated protists all
I
:
RNA
are especially important trophic links in these mi- Least squares analysis of ribosomal indi-
Archaea (Embley
crobial food webs in that they are major consumers cates two major groups of et al.,
of planktonic bacteria, pico- and nano-planktonic 1994). One branch, the Crenarchaeota, includes a
extreme
homogeneous group sulfur-dependent
other of
autotrophs, diatoms, dinoflagellates, ciliates,
and amoebae, and erm
and heterotrophic flagellates
A
more
they are eaten in turn by animals such as zooplank- is
energy by anaer-
ton and planktivorous larval fish (reviewed in (anaerobes with the ability to get
—
& methane an
biodegrading substances
obically to
Pierce Turner, 1992).
554
Annals
of the
Missouri Botanical Garden
economically
important biotechnology used world-
walls containing oniilhine In place of diami-
wide
both to reduce waste and generate fuel-grade nopimelic
acid in peptidoglycan.
its
—
biogas [Reeve, extreme
1992]), halophiles (Archaea 6. Spirochaetes this group, which was originally
living in high salt environments), and miscella- recognized on the basis of unique morphol-
its
neous
thermophiles
(Woese, 1987). This
classifi- nfirm
cation is controversial and has inspired a limited by analysis of rRNA.
—
DNA
debate over the best way analyze sequence Chlamydia group
to 7. this consists thus far of
data, as well as the appropriateness of relying on a only one genus. Chlamydia, whose members
single molecular sequence
(in this case the ribo- all intracellular parasites responsible for a
somal RNA) number
(see, for example. Lake, 1987, 1989; of sexually transmitted diseases and
&
Rivera Lake, 1992). Hopefully, as more data trachoma (a form of blindness).
—
from
different molecules are accumulated and sys- ^- Actinomycetales gram-positive bacteria which
may
lemalists of prokaryotes become more sophisticated form branching chains that superficially
resemble
about phylogenetic analysis, a better substantiated the filamentous bodies of fungi. They
hypothesis of archebacterial relationships are notorious for species that cause tubercu-
will
and
emerge. losis leprosy, but most are
free-living
soil
The microbes of interest pharmaceutical com-
true Bacteria, or Eubacteria, have a pepti- to
doglycan cell wall, membrane composed panies for their ability to produce antibiotics
lipids of
straight carbon chains attached by that retard the growth of other bacteria.
to glycerol ester
—
9. Proteobacteria this large, diverse group
arm in-
quence of tRNA, and they use formylmethion- cludes the puqile sulfur bacteria and their rel-
th<'
Many
atives. of the organisms group
ine as a start signal for protein synthesis. Neighbor in this arc
phototrophic and use the pigment bacterio-
joining analysis indicates
that there are ap[)roxi-
which
clilorophyll, absorbs longer wavelengths
mately 13 groups of eubacteria (Embley
et al..
than other chlorophylls. has been hypothe-
1994) been It
surveyed.
sized (but not yet rigorously tested using phy-
those needing
further investigation are temporarily
logenetic methods)
that the ancestor of this
placed
in descriptive categories rather than formal
group was photosynthetic and
that physiologi-
taxa:
cal diversity characteristic of the group arose
—
as a result of the exchange of photosynthetic
Aquifex-Hydrogenbacter organisms
1.
that oxi-
capacity
for other physiological processes
dize reduce compounds
or sulfur extreme
H;,
at
(such as sulfate reduction) as the bacteria ex-
temperatures Some
(up to 95°C). authors have
panded new
The
into ecological niches. group
suggested may
that these be phylogenetically
thus contains
a diversity of bacteria including,
interme<liate between remaining
the bacteria
in addition to the purple bacteria, sulfate- and
and
the Archaea.
—
sulfur-reducing
bacteria, fruiting myxobacteria,
Thermologales
2. two genera from geothermally
enteric bacteria, free-living and symbiotic N^-
heated marine
sediments.
and
fixers, sulfide-oxidizing
taxa.
3
—
or
Ifur Jih a 1-
Bacleroides-FJavohaclerium
1 0. this group con-
^fl
sists of several genera forming a major clade
ermo
t\
i
of gram-negative bacteria. includes a mix-
It
nonphototrophic.
—
ture of physiological types including
obligate
Planctomycetales
4. this group contains bud-
anaerobes
Bacteroides) and
(e.g., obligate aer-
ding organisms
that are often found attached
obes
(Sporocytophaga).
—
surfaces by These
to holdfasts. organisms have
11. Gram-positive bacteria with low C-f-C%
in-
some
unusual
features for bacteria; at least one
eluded here the endospore formers,
lactic
species has membrane-bound
a nucleoid
rm
&
rRNA
Webb,
(Fuerst 1991), and their operon
and mycoplasms.
teria,
—
from
is different other bacteria in that the 16S
12. Cyariobacteria the blue-g algae, like eu-
&
and 23S
genes
are separate (Liesack Stacke-
karyotic plants, use chlorophyll a and two pho-
brandt, 1989; Liesack 1992)
et
al., losystems tandem
— in to transfer electrons from
Deinoccaceae/Thermus
5, this group includes NADP+
water
to releasing 0^ as a waste prod-
just two genera: the radiation Deino-
resistant
uct.
—
and
coccus the chemoorganotrophic thermo-
Green
13. sulfur bacteria these bacteria are pho-
phile ThermiLS, both of which have
atypical
cell tosynthetic but use only one photosystem
to
555
Volume Number 4 Lipscomb
83,
1996 Microbial Diversity
and
transfer electrons from H^S (rather than water) the green plants, the choanoflagellates the
NADP^. sponges, or the chrysophytes and the multicellular
to
brown (Lipscomb, Not unicellular
That these groups are natural phylogenetic lin- algae 1989). all
cages of Archaea and Bacteria needs to be forms are related to one of the multicellular king-
still
some
tested with cladistic analysis. Furthermore, the doms. There is evidence that unicellular taxa
rRNA
molecule the kinetoplastids, euglenoids, or ciliates) are
ability of the to give significant (e.g.,
support for the deep branches of these trees needs independent lineages and not related to the multi-
be cellular organisms, and these forms should be
investigated.
to
own taxonomic
placed separate categories.
in their
become commonly used
Thus, has clear that
it
EUKARYOTE
DIVERSITY
schemes and
5-kingdom traditional
classification
Unicellular eukaryotic microorganisms are usu- categories (such as zooflagellate, phytoflagellate,
For many and sarcodine) are oversimplified and simply in-
ally collectively referred to as protists.
complained an under- adequate for describing the true nature of diversity,
years, protistologists that
and multiple kingdoms are needed.
standing of the phylogenetic relationships of the that
how many
eukaryotes was hampered by the pau- Determining what and of these cate-
unicellular
city of their fossil record and their microscopic size gories there might be is not easy (see history of the
These coming Lipscomb, 1991). Cladistic analyses of the
Corliss, 1974). barriers are field in
from and biochemical features of the cell
down, resulting in great research activity ultrastructural
confirmed
which a new picture of protist relationships is (Lipscomb, 1985, 1989, 1991, in prep.)
emerging. The reasons recent advances are two- the presence of at least thirteen major groups of
for
fold and obvious: First, with the widespread use of protists, all of which, incidentally, had been pro-
transmission electron microscopy, confocal micros- posed individually by earlier, more traditional sys-
and molecular genetic sequencing, micro- tematists Smith, 1951; Jeffrey, 1971; Leedale,
copy, (e.g.,
scopic size no longer a hindrance to gathering 1974; Edwards, 1976; Taylor, 1976, 1978).
is
character data on these organisms. In fact, unicel- Some of these groups have traditionally been
Algae
eukaryotic mitToorganisms possess a level of called algae because they are pholosynthetic.
lular
cellular and molecular diversity that far exceeds are not all phylogenetically related. In fact, the oc-
that found in multicellular eukaryotes, and this di- currence of at least six distinct lineages of algae
informat provides immediate evidence for their biodiversity
structing their phylogeny. Second, systematists (Andersen, 1992):
—
methods
have refined their empirical largely
—
The because
Rhodophyta, red algae, primarily
and 1.
thanks to the cladistic revolution is possi-
it
they can be multicellular and reach large body
new
ble to sort through and analyze the characters
considered be plants
sizes, are persistently to
meaningful ways.
in
many
by even though biology
biologists their
One major changes has emerged from
of the that
quite different from that of green plants.
group is
these studies the realization that the not
is
is
They are characterized by chloroplasts bound-
a cohesive, taxonomic group that stands as an an-
membranes
ed by two containing separate thy-
hub from which the other eukaryotic king-
cestral
lakoids and lacking an external coat of endo-
doms paraphy-
are derived. Instead, the protista
is
plasmic reticulum (Dodge, 1973; Pueschel,
monophyletic, and contains a hetero-
not
letic,
1989). They have chlorophyll a a- and B-car-
geneous mix of organisms at intermediate levels of ,
and zeaxanthin. Other pigments
otene, leutein,
organization and equivocal boundaries with multi-
A include the water-soluble allophycocyanin,
by
paraphyletic taxon united the
cellular taxa. is
phycocyanin, and phyrierythrin localized in
possession of shared primitive characteristics (sym-
phycobillosomes found on the thylakoids of the
plesiomorphies) rather than uniquely derived char-
and members thus do not have an- chloroplast. Floridean starch is the major stor-
acteristics,
its
and unique age product and found in the cytoplasm
unique themselves lack is
cestors to just it
rather than the chloroplast. This carbohydrate
individual histories (Hennig, 1966).
When unicellular forms are determined to be an has a primary chain of a-(l,4)-linked glucans
branched chain (Raven
grade along lineages leading mul- with a 1,6-linked et al.,
organizational to
ticellular taxa, the unicellular forms should be in- 1990). There are no flagella, centrioles, or bas-
Without
cluded in the group with their multicellular rela- al bodies (Pueschel, 1989). centrioles,
For example, there no kingdom-level is not surprising to find that mitosis in red
tives. is it
and
and from green algae
boundary between the unicellular chlorophytes algae is different that in
556
Annals
of the
Garden
Missouri Botanical
higher plants. The spindle forms on a unique some, and a periplast of proteinaceous plates
nucleus NAO),
associated organelle (called the underlying the membrane.
cell
which
is located on each division pole. Fur- 4. Chroniohionts {— Stramenopiles) are a group
thermore, the nuclear membrane does including both photosynthetic and
not heterotro-
down
break but remains intact except for small phic forms. These are the helerokont unicel-
openings organisms
at the pole for the spindle to pass lular with tubular cristae in their
through (Scott, 1983). Red algae have the old- mitochondria, mastigonemes in at least two
est fossil record of all the algae, with the ban- rows on one of the flagella, and a 6(l-3)-linked
giophytes found in 1.25-billion-ycar-old rocks glucan as a food storage product. Those forms
(Butterfield One cannot make that are photosynthetic have chlorophyll c\
et 1990). too a,
al.,
much and
of this because the fossil record for most c2, thylakoids in stacks of three, and four
membranes
surrounding
early eukaryotes very poor and some other the chloroplast with
is
membrane
may the outermost around
protist group have predated the red algae contiruiing the
nucleus.
but no record.
left
The
placement of the oomycete and hyphoch-
Chlorobionts. This clade represents one
2, of the
and
major groups ytrid fungi the labyrinthulids with the
of photosynthetic organisms.
It
chromobionts and was
not surprising sug-
includes the chlorophytes, charophytes, is
prasi-
nophytes, and gested by mycologists (e.g., Barr, 1981, 1992).
the multicellular plants. has
It
They
share with the Raphi<Iophyta a similar
been
also referred as the chlorophyte
to series
flagellar root structure that consists of a sheet
(Taylor, 1978) or the Viridiplantae (Cavalier-
of microtubules extending over the surface of
Smith, 1983). All of these taxa have chloro-
the nucleus. All these taxa share with the ga-
phylls a and and a-(l-4)-linked glucan (am-
h,
mete
of foraminiferans the presence of masti-
ylose/amylopectin)
as a food storage in their
gonemes
in two rows on the forward projecting
The
chloroplasts. chloroplast bounded by
is
flagellum and a naked trailing flagellum.
two membranes,
as in the rhodophytes, but the
Th(^ heliozoan Actinopodea appear be de-
to
thylakoids are in many-layered grana. Motile
rived from the chromobionts, from
specifically
cells with flagella have a stellate flagellar tran-
the chr}'sophyte order Pedinellales. The Helio-
region and
sition a cruciate flagellar root sys-
zoa were traditionally considered be sarcod-
to
Most
tem. unicellular chlorobionts have a
cell
ines because they have pseudopodia. These
made
wall or scales, but not always of cellu-
pseudopods,
usually called axopodia, are long
lose.
and slender and are made rigid by a core of
3. Cryplophytes (= Crj'ptomonads) can b e cnhar-
microtubules.
Ultrastructurally identical struc-
acterized as having chlorophyll a and phy-
r^^,
tures form an anterior ring around the
flagella
and
cobillins, the xanthopliyll alloxantin
in
of the Pedinellales. Thus, presence axopodia
of
chloroplasts surrounded by meml)ranes
four
synapomorphy
is a that unites the Heliozoa
and thylakoids in stacks of two. The inner pair
with the chrysophytes. This relationship has
membranes
of forms the plastid envelope and
been reported before by protozoologisls
(e.g.,
the outer pair forms the plastid endoplasmic
Patterson, 1989) but often ignored by phycol-
reticulum. There an expanded space be-
is
ogists.
tween
the plastid endoplasmic reticulum and
Loosely allied with the chromobionts are the
plastid envelo[)e on one This expand-
tlie face.
Eustigmatophyta and The
the bicoecids. Eus-
ed area contains ribosomes, and
starch grains,
tigmatophyta
are photosynthetic and, as with
the nucleomorph unique double membrane
(a
memb
other chromobionts, they have four
bound DNA). The
structure containing nucleo-
surrounding
their chloroplast with thylakoids
morph been
has postulated to be a vestigial
in stacks of three and two rows of mastigone-
nucleus belonging
to a photosyntht^tic eukary-
mes
on one However,
flcigellum. there only
is
&
otic symbiont (Ludw^ig Gibbs, 1987; Douglas
chlorophyll a (no c) and the outermost chloro-
The
et al., 1991). food storage is the a-(l-4)- membrane
plast not continuous with the nu-
is
linked glucan glycogen, and
it is stored in the clear membrane. Whetlier the eustigmatophy-
nucleomoiph. The mitochondrial
cristae are
tes are primitive chromobionts or derived forms
The
flattened tubes. flagella have tubular mas- many
with secondary losses cannot be
deter-
tigonemes in two rows on one flagellum and mined The
at this time. colorless, phagotrophic
one row on They
the other. also possess a bicoecids have been considered be
to related
unique extmsome,
called the refractile ejecto- to the chromobionts by other protistologists be-
557
Volume Number 4 Lipscomb
83,
1996 Microbial Diversity
cause they also have two rows of mastigonemes brous roots. They also possess two kinds of nu-
on one flagellum, and their flagellar root struc- clei: a micronucleus that functions in genetic
gametes brown exchange, and a macronucleus that functions
ture similar to that of the of
is
algae and the xanthophyte Vaucheria (Moestrup in protein synthesis.
&
Thomsen, 1976). However, they have The Apicomplexa are all symbiotic and in-
evolved many unique features that are perhaps elude many major disease-causing organisms
The
obscuring information that would allow us to (e.g., Plasmodium, which causes malaria).
place them definitively as the sister taxon to anterior end of the cell contains a unique corn-
presumably function
one of these chromophyte groups. plex of organelles that in
and
Euglenozoa. The euglenids and the kinetoplas- attachment penetration of the hosts' cells,
5.
were recognized as related The remaining groups consist almost exclusively
tid flagellates first
Many
have
taxa by Leedale (1967). The morphological fea- of heterotrophic organisms. of these
mode
tures these taxa share include linked micro- been called protozoa, but this shared of nu-
tubules underlying the cell membrane, and trition is not sufficient to unite all of these forms
Some
taxonomic
discoidal cristae in the mitochondria. into a category.
members Euglenida Euglenophyta
of the (or in
These
Parahasalida, heterotrophic flagellates
7.
and
the botanical literature) are autotrophic
possess a distinctive flagellar root structure,
all
possess chlorophyll a and has been hy-
b. It
which includes a rod of microtubules that ex-
rem-
pothesized these chloroplasts are the
that
tends from the basal bodies around the surface
nants of endosymbiotic chlorobionts or chlo-
An
nucleus (= elaborate stack
of the axostyle).
What-
robiont chloroplasts (Lefort-Tran, 1981;
of golgi vesicles often associated with this
is
many
1981). Like chlorophyte chloro-
ley,
between the nucl and the basal bodies.
root
plasts, those of the euglenids lack light-har-
These are almost exclusively symbiotic
protists
vesting carotenoids (Rowan, 1989) and a girdle
many Some
and are found in different hosts.
lamella. In addition, each chloroplast sur-
is
species, such as Trichomonas, are parasites of
membrane
rounded by an additional single
humans, but other species, such as Barbula-
which
(Dodge, 1973), consistent with the
is
nympha
and Trichonympha, inhabit termites
remnant symbionts. Euglen-
idea that they are
and woodroach Cryptocercus where they aid
the
have a unique storage product, paramylon,
ids
the digestion of cellulose.
in
which a 6 (l,3)-linked glucan chain stored
is
Metamonadida. The majority of these flagellat-
8.
Phagotrophy
cytoplasm.
as grains in the is
ed symbionts Giar-
protists are intestinal (e.g.,
common
and
both pholosynthetic colorless
in
some They were once
but are free-living.
dia),
forms, and the microtubules associated with
thought to be closely related to the parabasa-
the base of the flagella play a role in feeding
& ans wi wl10m they sh the absence of mi-
ith
(Triemer Farmer, 1991). I
tochondria and storage glycogen, but they lack
The and Ciliophora
Dinoflagellata
Alveolates.
6.
The
the axostyle and golgi apparatus. meta-
have been linked as sister taxa on the basis of
monads are characterized by the presence of
an alveolar membrane system and the presence
three bands of microtubules associated with
of microtubules lining the cytopharynx. Be-
membranes, the base of their flagella: a supranuclear band,
cause they also have alveolar the
an infranuclear band, and a band paralleling
Apicomplexa included
parasitic are also in this
membrane the recurrent flagellum and oral inpocketing.
lineage. This alveolar system con-
membrane-bound 9. Animals. The taxa that are included in the an-
of a layer of sacs lying
sists
which
membrane. imal clade are united by mitosis in
beneath the plasma In the di- all
just
the nuclear membrane breaks down by frag-
noflagellates, these alveoli contain the theca.
choanocytes,
Some and mentation, septate junctions, col-
dinoflagellates are photosynthetic so
sometimes These photosyn- lagen, spermatozoa, and basal bodies at right
are called algae.
forms contain chlorophyll a and com- angles to each other in flagellated cells. Group-
thetic C2
plexed with a unique xanthophyll, peridinin. ing with the animal taxa are a protozoan taxon
The Ciliophora make up one of the largest (the choanoflagellates) and the Chytridiomy-
The grouped
groups of protists and, as has already been dis- cota (chrytid fungi). chytrids are
cussed, play a major role in microbial food with the sponges and choanoflagellates be-
webs as predators and bactivorous organisms. cause all have microtubules radiating perpen-
which
Ciliates generally have rows of cilia with a dicularly to the basal body, are inter-
unique system of two microtubular and one connected by concentric rings of electron-
fi-
558
Annals
the
of
Garden
Missouri Botanical
dense
material (Lipscomb, 1989, 1991; Barr, adapted to intracellular parasitism. But some
1992). have mean
interpreted this to that the micro-
Although additional data is needed to be cer- sporidians are direct descendants of primitive
tain, it is probable that the Myxozoa, a group eukaryotes (e.g., Cavalier-Smith, 1993).
of protists with multicellular spores and spe- In conclusion, a new classification consisting of
cialized structures called polar capsules, will at least 13 groups of eukaryotes emerging, but a
is
belong to the animal lineage. Like the true robust phylogeny of the eukaryotes will not be re-
metazoans, they have a separation of somatic solved until more taxa are examined with both mor-
and germ and The
cells cell junctions. polar phological and molecular techniques.
First, cell bi-
many
capsules share
striking characteristics ology, particularly electron microscopy, has
with the nematocysts of cnidarians (Lom, provided the basic data on which this multi-king-
1990), and these similarities appear to be syn- dom system based, and many of these characters
is
Myxozoa
aponiorphit\s that unite the with the turn out to be convergent, or reversed, or both. For
cnidarian clade. this reason, some branches are defined by very few
10. Amoeboflagellates. Tlie amoeboflagcUates and characters and cladograms have several unresolved
the cellular slime molds form a clade in which branch points where several lineages appear
to di-
the taxa form limax amoeba that move rela- verge simultaneously rather than form a more
in-
tively rapidly by the production of eruptive formative branching pattern. Second, analyses do
pseudopodia
that lack fine extensions. This re- not yet include many parasitic and structurally
been
lationship has suggested by other proto- unique forms. Thus they do not address phyloge-
The
zoologists (Page, 1976). amoeboflagellates placement
neti(^ of of the taxa.
all
are also able to transform to a flagellated stage.
The
11. Rhizopods. rhizopods with blunt lobose
CONCLUSION
pseudopodia can be only tentatively grouped
^"
appreciation and understanding
of the natu-
They
together. have a simple cell structure and
world depends on
many ral a description of the systematic
lack of the characteristics used in the
^"^^ ecological diversity of microorganisms as well
As
cladistic analysis. the analysis expanded,
is
we may ^^ better-known plants, animals, and fungi,
discover group '^^^
that this polyphylet-
is
There can be doubt
that the biodiversity of
little
ic.
and mif^roorganisms poorly known. Yet as our
12. Opaliniih Proteromonads, These possess is still
knowledge has grown has become increasingly
similar arrays of subpellicular microtubules it
underlying membranes ^^^^^ ^^at these organisms are an essential and dl-
the folds in their cell
and a unique form of pinocytotic heterotrophy. ^^^^^ P^^ ^^ ^^e ecosystems of the world.
Th
& no consensus on the phylogenetic
Mignot (cited in the paper by BrugeroUe Joy- is re-
lationships of the various unicellular organisms
was at
on, 1975) the protozoologist suggest
first to
phylum and kingdom new
^^^ level and, as long as
that these forms were related.
^^^^ ^"^ characters are discovered, innovations
The members in
13. Microsporidia, of this group have
kingdoms
number classifications of the will likely continue,
a
of features that are not apparently
obvious
that classifications that divide organ-
homologous features found other ^^ *^
to in protists.
kingdoms
They '^"^^ ^"^0 just two, three, four, or five
are small (2-7 \Lm) intracellular parasites
many ^^^ simplistic, and a multi-kingdom system pro-
that infect kinds of eukaryotes, including
^ "^^^e realistic view of the diversity of
other protists. The spore the developmental ""'^'^^"^ life,
is
Concomitant some
with this the realization that
stage with the longest duration, and at the light is
traditional categories such as monera, algae, pro-
microscopic
level the only cycle stage
Is life
it
^^^^^' ^^ ^^"8^ ^'^" "^ Xon^^^r be considered distinct
that can be identified as belonging a miero-
to
An
phylogenetic groups. overall scheme of classi-
sporidlum. Not surprisingly then, most of our
fixation that reflects our growing databases has not
morphological information comes from
the
completely emerged. Undoubtedly,
not
spore stage, which has a characteristic polar X^^ it will
resemble many
tube and cap used sporoplasm those followed in textbooks today,
to inject into a
more
where can grow and ^^"^ ^'^^ re^ei:X accurately the relationships
host cell divide. Phy- '^
it
rRNA unicellular microorganisms.
^^ ^^^^
logenetlc analysis of the small subunit
en shnows microsponcnans
oft tthne idi adiiverguig
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