Despite being
unicellular, diatoms are highly organized cells, presenting complex sexual
reproduction processes, characterized by a common scheme.
Life Cycle
Diatoms are diplonts
with meiosis in the final stage of gametogenesis (figure below). The duration
of the haploid phase is relatively short, not exceeding several hours, while
the diploid state may last from months to years, depending on the species and
the environmental conditions. The life cycle of diatoms is thus composed of two
successive phases: a prolonged phase of vegetative multiplication and a very
short period of sexual reproduction.
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| Different Types of Life Cycles Explored by Algal Groups and other Organisms. |
Depending upon the
precise time and purpose of meiosis and gamete fertilization in the cycle, one
can discriminate between haplontic life cycles (also called zygotic meiosis
life cycles since meiosis occurs during germination of the zygote, the dominant
part of the life cycle is haploid) or diplontic life cycles (also called
gametic meiosis life cycles as meiosis is used to produce haploid gametes, the
dominant part of the life cycle is diploid). Haplo-diplontic (= diplobiontic)
life cycles (also called sporic meiosis life cycles as meiosis is used to
produce haploid spores) represent a combination of both, with the gametophyte
stage producing gametes and the sporophyte producing spores. Microscopic algae
use zygotic (e.g., dinoflagellates), gametic meiosis (diatoms), or sporic
meiosis (haptophytes). Sessile macroscopic seaweeds experiment (at least
functionally) gametic or sporic meiosis, which ultimately is utilized by all
land plants.
Vegetative
multiplication is performed through common mitotic division. Under any
circumstances, the biggest cells cannot reproduce sexually. However, most
diatoms undergo significant size reduction over their life cycle, a phenomenon
that puzzles many novice analysts of plankton samples. This happens because of
the specific structure of the diatom cell wall also known as the frustule. The
silicate frustule is rigid and consists of two parts, the epitheca and the
hypotheca, which are joined to each other in a manner similar to the base and
lid of a Petri dish. During mitotic division both daughter cells acquire new
‘bases’, i.e., hypothecae. As a result, after each act of vegetative
multiplication via mitotic division one daughter cell keeps the parental size,
while the other daughter cell becomes a little bit smaller in length (in
pennate diatoms) or diameter (in centric diatoms). As cells divide, the mean
cell size in a particular population gradually decreases, a phenomenon known as
the MacDonald-Pfitzer rule (MacDonald 1869; Pfitzer 1869).The shift from the
vegetative to the sexual phase of the life cycle in diatoms is size dependent.
Upon reaching a critical size threshold, which is species specific, cells
becomes sexually inducible and may enter sexual reproduction. It is not
obligatory for cells below a critical size threshold to enter sexual
reproduction, they are just allowed by the size factor to do this; many cells
in the population continue vegetative multiplication. In some species there is
also a second threshold below which cells could again not be induced to become
sexual but rather divide mitotically until they die. When favorable conditions
combine, such as the proper cell size, availability of the sexual partner (if
needed), suitable environmental factors (light conditions, temperature,
salinity, etc.), and cells may shift from mitotic to meiotic division. The
cells produce gametes, and can therefore be named gametangia. The process
results in the reduction of the chromosome number to half that of parent cells
(i.e., haploid). Gamete fusion leads to zygotes, restoring the diploid state.
Zygotes commonly start to grow without any dormancy period. At this stage, the
cells, which are called auxospores, are not surrounded by a siliceous frustule
and are thus capable of expansion. The auxospore typically expands very
quickly, reaching the maximum (or close to maximal) species specific size in a
couple of hours. However, auxospore growth is not simple swelling of the cell
and concomitant expansion of the cell wall; a more or less complex structure
composed of silicate scales, rings and bands is formed in the growing cell as a
skeleton, named in pennate diatoms as the perizonium.
The deposition of
perizonial bands causes the rupture of the primary zygote wall (the membrane
surrounding the zygote) and the remnants of such a membrane can be seen in many
cases on both tips of the elongating auxospore in the form of caps. As soon as
the auxospore has reached the maximum size, the diploid nucleus undergoes an
acytokinetic division that precedes the deposition of the two initial valves
(epitheca first, followed by hypotheca) inside the fully-grown auxospore. As a
result, a new cell of the biggest size (an initial cell) arises. The initial
cells may differ more or less from the vegetative cells in shape and structure
of silica frustules. After being released from the auxospore envelope, the
initial cell resumes vegetative multiplication and thereby creates a new clonal
lineage of cells, which are renovated genetically and have the biggest sizes.
The close relationship
between sexual reproduction and cell size restoration is an intriguing feature
of the diatom life cycle. In a few species vegetative enlargement has also been
observed (Gallagher 1983; Nagai 1995; Chepurnov et al. 2004). Usually,
auxosporulation occurs in conditions that are favorable for vegetative growth.
Certain centric and pennate diatoms can form resting stages in response to
environmental stress (for details see Round et al. 1990). Nevertheless, in most
cases the transition to dormant stages such as resting spores/cells or winter
forms is not a typical characteristic of the diatom life cycle and is
obligatory only in a few species (e.g., French and Hargraves 1985).
 |
Diagrammatic Representation of
the Life Cycle in a Centric Diatom Melosira sp. (a) an initial cell formed in a
mature auxospore, (b-f), because of specifi c construction of the frustule the
cell size decreases while cells pass through mitotic cycles, (g) male and (h)
female gametogenesis; n and 2n, haplontic and diplontic phases (cell diameter
range ca. 20–80 µm).
|
Generically, if
compared with other groups of algae, ‘lower plants’, higher plants, and
vertebrates (Mable and Otto 1998), the diatoms have a life cycle similar to
those of the evolutionarily most advanced organisms (figure above). In contrast
to many other algae, where closely related taxa can exhibit widely variant life
cycles with respect to the duration of haploid and diploid phases, the life
cycle strategy in diatoms appears to be more permanent and uniform.
Patterns of sexual
reproduction
A great diversity of
copulation processes has been revealed in diatoms. Centric diatoms (Figure
below) were shown to be oogamous (von Stosch and Drebes 1964; Schultz and
Trainor 1968); they produce large non-motile female gametes (eggs) which are
fertilized by small motile flagellated male gametes (sperms). Male cells
usually undergo a series of successive differentiating mitoses giving rise to a
variable number (2, 4, 8, 16, and 32) of small diploid spermatogonia, which
complete their further development by sperm formation (spermatogenesis). Two main
types of spermatogenesis are known, depending on the formation of residual
bodies, the merogenous and the hologenous types. The flagellum of the sperm
cell is directed forwards during swimming and does not conform to the usual
eukaryotic 9+2 arrangement, but shows a 9 + 0 pattern, i.e., central
microtubules are lacking (Manton and von Stosch 1966; Heath and Darley 1972).
In contrast to the spermatogonia formed by de-pauperizing mitoses, the oogonia
usually develop directly from vegetative cells. Three types of egg formation
are recognized: (1) oogonia containing two eggs, (2) oogonia containing a
single egg and a polar body, (3) oogonia containing a single egg. Independent
from the meiotic nuclear stage of the oocyte, fertilization may happen as soon
as the egg surface is mechanically (partly or totally) exposed, but in all
cases nuclear fusion (karyogamy) does not follow before the female nucleus has
reached the mature haploid stage (Drebes 1977). As a rule during fertilization
the flagellum is discarded. Unlike centric, gametes released by pennate,
diatoms are more or less equal in size (isogamy), however, they may differ
morphologically and behaviorally depending on the species (see image below).
Taken into account these and many other details, Geitler elaborated a
comprehensive system of sexual reproduction patterns (Geitler 1973; Mann 1993).
What is important, a flagellate stage has never been described in pennate
diatoms (see also discussion in Subba Rao et al. 1991, 1992; Rosowski et al.
1992; Davidovich and Bates 1998). Automixis in the form of paedogamy or
autogamy is also possible; and some diatoms are known to be apomictic (Geitler
1973; Vanormelingen et al. 2008).
 |
Diagrammatic Representation of
the Life Cycle in the Pennate Diatom Haslea karadagensis. (a) an initial cell,
(b-e) vegetative cells passing through mitotic cycles, (f) pairing of
gametangia, (g) gametogenesis, (h) zygotes, (i-j) auxospore formation; n and
2n, haplontic and diplontic phases (cell length range: ca. 20–95 µm).
|
Generically, if
compared with other groups of algae, ‘lower plants’, higher plants, and
vertebrates (Mable and Otto 1998), the diatoms have a life cycle similar to
those of the evolutionarily most advanced organisms (figure above). In contrast
to many other algae, where closely related taxa can exhibit widely variant life
cycles with respect to the duration of haploid and diploid phases, the life
cycle strategy in diatoms appears to be more permanent and uniform.
Patterns of sexual
reproduction
A great diversity of
copulation processes has been revealed in diatoms. Centric diatoms (Figure
below) were shown to be oogamous (von Stosch and Drebes 1964; Schultz and
Trainor 1968); they produce large non-motile female gametes (eggs) which are
fertilized by small motile flagellated male gametes (sperms). Male cells
usually undergo a series of successive differentiating mitoses giving rise to a
variable number (2, 4, 8, 16, and 32) of small diploid spermatogonia, which
complete their further development by sperm formation (spermatogenesis). Two main
types of spermatogenesis are known, depending on the formation of residual
bodies, the merogenous and the hologenous types. The flagellum of the sperm
cell is directed forwards during swimming and does not conform to the usual
eukaryotic 9+2 arrangement, but shows a 9 + 0 pattern, i.e., central
microtubules are lacking (Manton and von Stosch 1966; Heath and Darley 1972).
In contrast to the spermatogonia formed by de-pauperizing mitoses, the oogonia
usually develop directly from vegetative cells. Three types of egg formation
are recognized: (1) oogonia containing two eggs, (2) oogonia containing a
single egg and a polar body, (3) oogonia containing a single egg. Independent
from the meiotic nuclear stage of the oocyte, fertilization may happen as soon
as the egg surface is mechanically (partly or totally) exposed, but in all
cases nuclear fusion (karyogamy) does not follow before the female nucleus has
reached the mature haploid stage (Drebes 1977). As a rule during fertilization
the flagellum is discarded. Unlike centric, gametes released by pennate,
diatoms are more or less equal in size (isogamy), however, they may differ
morphologically and behaviorally depending on the species (see image below).
Taken into account these and many other details, Geitler elaborated a
comprehensive system of sexual reproduction patterns (Geitler 1973; Mann 1993).
What is important, a flagellate stage has never been described in pennate
diatoms (see also discussion in Subba Rao et al. 1991, 1992; Rosowski et al.
1992; Davidovich and Bates 1998). Automixis in the form of paedogamy or
autogamy is also possible; and some diatoms are known to be apomictic (Geitler
1973; Vanormelingen et al. 2008).
Delivery of the Gametes to
the Place of Syngamy
The whole content of
the gametangial cell transforms into only one or two gametes (more in centric
males). Therefore, the cost of sex is very high in diatoms (Lewis 1984).
Several mechanisms that promote the encounter of gametes and thus their fusion
have evolved. Oogamous fertilization in centric diatoms is effective because of
motile male gametes; they swim by being dragged and not pushed by the anterior
flagellum. Very often, the gametes of the raphe-bearing pennate diatoms are
brought together by a prior pairing of their mother cells (gametangia) of the
complementary sexes. For this reason the term ‘gametangiogamy’ is also in use
(Wiese 1969).
To secure
fertilization, in several benthic pennates a mucilage capsule is secreted
around the copulating partners. Once gametangia are physically close, another
type of active movement, amoeboid movement may be employed. This movement
allows gamete transfer to the place of syngamy and is sufficient for short
distance translocation of the gamete from closely positioned gametangia.
Vegetative cells of a very diverse group of araphid pennates, however, are
sessile and only a few species are known for their slow motility (Kooistra et
al. 2003; Sato and Medlin 2006). An unusual mechanism of male gamete motility
has recently been described in araphid pennates, involving formation of
thread-like cytoplasmic projections on the gamete cell surface (Sato et al.
2011; Davidovich et al. 2012).
Factors triggering sexual
reproduction
If mating is
heterothallic, interaction between sexual partners is required to initiate
meiosis and gametogenesis. There is some evidence that the process of
sexualisation is triggered by a sophisticated multi-stage exchange of several
pheromones (Sato et al. 2011; Gillard et al. 2012). For now, it is unclear how
species-specific these pheromones are. If pheromones or their combination are
unique for each species, a minor change in their structure may lead to certain
problems in the control of cell pairing that predetermine a very short and
efficient way for speciation in diatoms, even in sympatric populations.
Comprehensive
observations gained by previous investigators, mainly by Geitler (Geitler
1932), allowed Drebes to write in his review (Drebes 1977, p. 271): “In
contrast to other protists, induction of sexualisation in diatoms depends not
only on the genotype and specific environmental conditions but also on a
suitable cell size as an internal non-genetic factor”. The concept of ‘cardinal
points’ in the life cycle of diatoms developed by Geitler (Geitler 1932)
declares that cells cannot be induced to become sexual until they have declined
in size below the critical size. The upper threshold for sexual induction can
range from 30% to 75% of the maximal size of the initial cells. However, for more
than half of the species examined, the threshold was at 45% to 55% (Davidovich
2001).
Apart from suitable
cell sizes, one of the necessary conditions for successful sexual reproduction
is an excellent physiological state. Laboratory practice has shown that the
best results can be achieved in exponentially growing cultures. Stressed
cultures never undergo sexual reproduction (Chepurnov et al. 2004). Beside
internal cues, a number of external factors have been shown to influence sexual
reproduction in diatoms (Drebes 1977). Appropriate light conditions are highly
important, sometimes being a key factor in triggering sexual reproduction
(e.g., Hiltz et al. 2000; Mouget et al. 2009).
Mating System
While centric diatoms
are believed to be genetically monoecious and hence are capable of homothallic
reproduction (Drebes 1977; however see comments in Chepurnov et al. 2004),
pennate diatoms are for the most part heterothallic, or combine homo- and
heterothallic modes of sexual reproduction (Roshchin and Chepurnov 1999;
Chepurnov et al. 2004; Davidovich et al. 2009, 2010; Amato 2010). In the case
of strict heterothally (genetic dioecy) clones are divided into two mating
types, which are usually indistinguishable at the stage of vegetative growth,
but in certain species may clearly differ by morphology and/or behavior of
their gametes (e.g., Stickle 1986; Davidovich et al. 2009). These diatoms
(cis-anisogamous sensu Mann 1982) are most suitable as model species for
studies of sex determination and sex inheritance. If differences are visible
and correspond to two mating categories, these can be designated as ‘male’ and
‘female’. Otherwise, mating types are conventionally termed plus and minus, ‘+’
and ‘–’.
Sex Determination
Mechanism of sex
determination in diatoms is poorly understood. Sex chromosomes are unknown, at
the same time obligate heterothallic reproduction and existence of two mating
types in some pennates suggest genetic dioecy. In such a case sex factors must
be located on different chromosomes. It has been shown that sibling clones,
derived from the two initial cells formed during sexual reproduction of a
single pair of gametangia (in those species where each gametangium produces two
gametes) were of opposite sexes (Mann et al. 2003). This and other experiments
(e.g., Chepurnov and Mann 2004) indicate that sex determination in
heterothallic pennate species is not developmental or phenotypic.
Sex differentiation is
impossible in the case of automictic reproduction, but automixis is not common
among diatoms. A genetic base for sex determination can be reasonably
elucidated in those species which are able to reproduce both intra- and
interclonally. The mode of sex inheritance revealed in a homothallic progeny
may give an answer to the question of how sex factors are distributed
(Davidovich 2002; Chepurnov et al. 2004; Davidovich et al. 2006). Data acquired
suggests coupling of chromosomes bearing male (M) and female (F) genetic
factors in combinations MF and FF for male and female sexes accordingly. Male
sex is thus heterogametic.
However, it cannot be
ruled out that this simple model will prove to be more challenging as more data
become available. For example, in several pennate diatoms some clones behaved
as males when mated with female clones, but as females when mated with male
clones (Chepurnov et al. 2004); this suggests mating system to be more complex
than the bipolar and obscures the sex determination mechanism.
An example of
phenotypic sex determination can be found in centric diatoms (Drebes 1977),
where sex appearance generally depends on the stage of the life cycle. In one
and the same clone, relatively big cells recently entered into the sexual size
region produce eggs, while getting smaller they shift to spermatozoid
production. At the same time, in some centric diatoms there were particular
clones which acted as ‘pure’ males, never producing female gametes (Chepurnov
et al. 2004).
Asexual auxosporulation
Auxospore formation is
usually regarded as a process intrinsically connected with the phenomenon of
sexual reproduction. However, sometimes auxospores may occur in the absence of
any sexual process (e.g., Nagai et al. 1995; Sabbe et al. 2004; Chepurnov et
al. 2004). Apomixis treated as diploid parthenogenesis is associated with
asexual auxosporulation, and was reported both in centric and pennate diatoms.
In other cases, unfused gametes can transform into auxospores (haploid
parthenogenesis). The last is facultative in some allogamous pennate diatoms.
During vegetative cell enlargement noted in some diatoms (e.g., Gallagher 1983;
Nagai et al. 1995) the cells escape from the ‘trap’ of critical size
diminution, but cells developed directly from vegetative cells do not produce
typical perizonium and their size is approximately half the size of the normal
auxospores produced by the same clone.
#Diatoms #Microalgae #Reproduction #AsexualReproduction #SexualReproduction #BinaryFission #Meiosis #Gametes #Frustules #Mitosis #CellDivision #GeneticDiversity #MatingTypes #Isogamy #Anisogamy #Haploid #Diploid #Zygote #EnvironmentalAdaptation #GeneticRecombination #Bacillariophyta #AlgaeLifeCycle #DiatomReproduction #SilicaCellWalls #DiatomEcology #AquaticMicroorganisms #MarineLife #BiologicalReproduction #EcologicalSuccess #MicroscopicLife
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