Abstract |
The present thesis investigates two aspects of phytoplankton ecophysiology, which are particularly
important in oligotrophic aquatic ecosystems. The first aspect is related to the
mechanism of excretion of dissolved organic matter by photosynthetic cells, under varying
nutrient availability conditions. The second aspect refers to mixotrophy in pigmented
nanoflagellates (PNF) which is defined as the combination of autotrophy through photosynthesis
(phototrophy) and heterotrophy through phagocytosis of bacteria (phagotrophy). The
results of the present study emerge from the combination of theoretical and experimental
approaches.
In order to better understand the processes of dissolved organic matter (DOM) release by
photosynthetic cells under nutrient-replete and nutrient-limited conditions, a model based
on Dynamic Energy Budget (DEB) theory is developed. In the context of DEB theory, two
alternative pathways of DOM release emerge from the theory; one relates to growth and
lysis of the cells and one to rejection of unprocessed substrates due to stoichiometric constraints.
These pathways represent the two conceptual mechanisms of DOM release, which
are the passive diffusion and active exudation, respectively. The relative contribution of the
two mechanisms to DOM excretion depends on nutrient availability and affects the quality
of produced DOM in terms of elemental and molecular composition and size fractionation,
which, in turn, may have implications for the bioavailability of the produced DOM to bacteria.
Focusing on mixotrophy among PNF, a general modelling framework is developed for
describing the nutritional strategies in four types of mixotrophic PNF. The resulting mathematical
expressions are incorporated in the aforementioned DEB model for photosynthetic
cells. The resulting models describe explicitly, for the first time, the functional diversity
of the PNF assemblage taking into account the dynamic interaction of phototrophy and
phagotrophy within the four types of PNF. Simulations suggest that the growth dynamics of
the four types of PNF are affected differently by the availability of resources (light, dissolved
inorganic nutrients and bacteria). A comparison of the rates of organic carbon production
and prey consumption by the various PNF types shows that their net ecosystem role, as
producers or consumers, depends on the mixotrophic strategy and it can vary as a function
of the prevailing environmental conditions.
Moreover, in the present thesis, an in-depth investigation of mixotrophy among PNF
in the ultra-oligotrophic, phosphorus (P)-limited Eastern Mediterranean Sea (EMS) is performed,
employing a two-phase experimental study that combined both field and laboratory
nanoflagellates grazing experiments. During the field experiments, the abundance, and
grazing effect of pigmented (PNF) and heterotrophic (HNF) nanoflagellates on prokaryotic
picoplankton stock (i.e., heterotrophic bacteria (HB) and Synechococcus) were assessed in
April 2016 at four stations in the NW Levantine sea and at two selected depths representing
the surface and the deeper (deep chlorophyll maximum) euphotic layer. Results showed that
HNF dominated prokaryotic picoplankton consumption in the surface layer, whereas, PNF
were the dominant grazers of prokaryotic picoplankton in the deeper euphotic layer. A negative
relationship between phosphate concentration and ingestion rate of PNF on prokaryotic
picoplankton was observed. Subsequent microcosm experiments were performed with nutrient
depleted water from the Cretan Sea (EMS) during the late stratified season, in order
to asses the responses of heterotrophic and pigmented nanoflagellates, in terms of bacterial
grazing, when relaxing the observed P-limitation. In accordance with the results of the field
experiments, PNF ingestion rate of heterotrophic bacteria (HB) was significantly reduced in
the P-amended treatment, whereas for HNF this rates remained unaffected by P-addition.
PNF dominated bacterivory in the unperturbed (control) bottles, whereas, in the P amended
treatment HNF and PNF contributed equally to total bacterivory. The experimental results
obtained in the present study emphasize the significant and P-dependent role of PNF as
consumers of HB in the EMS.
The results of the theoretical and experimental work undertaken in the present thesis are
synthesized into an idealized microbial food web model. This theoretical analysis aims to further
explore qualitatively the effect of phosphorus availability on the trophic interactions and
physiological processes of heterotrophic bacteria, heterotrophic and pigmented nanoflagellates
in the EMS. The model simulations suggest alternating pathways of P transfer through
the microbial food web components during P-replete and P-limited conditions. Pigmented
nanoflagellates hold a key role in P transfer through the trophic “by-pass” pathway sensu
Thingstad et al. (2005) [Thingstad et al., 2005. Science, 309:1068–1071] under P-limited
conditions, whereas the relative role of heterotrophic nanoflagellates in this pathway is more
prominent at P-replete conditions. The complicated interactions between PNF and HB in
the EMS could be conceptually described as an alternative microbial loop, in respect to the
established paradigm involving heterotrophic bacteria and HNF. In this alternative microbial
loop, PNF have the functional role of DOM primary producers, mainly through the active
exudation mechanism, and, at the same time, share with HNF the functional role of bacterial
consumers via mixotrophy. This alternative microbial loop in the oligotrophic system of the
EMS operates in a phosphorus-dependent way.
The results of this thesis emphasize the importance of the adaptive physiology of photosynthetic
protists for the functioning of oligotrophic systems and the importance of taking
into account this adaptive behaviour in biogeochemical models in order to predict the response
of oligotrophic systems to environmental changes.
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