Cycling of dissolved and particulate organic matter in the pelagic marine environment : Impact of phytoplankton community mortality and microbial degradation

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Title: Cycling of dissolved and particulate organic matter in the pelagic marine environment : Impact of phytoplankton community mortality and microbial degradation
Author: Elovaara, Samu
Contributor: University of Helsinki, Faculty of Biological and Environmental Sciences
Doctoral Programme in Wildlife Biology
Finnish Environment Institute
Tvärminne Zoological Station, University of Helsinki
Publisher: Helsingin yliopisto
Date: 2020-12-10
Language: en
Thesis level: Doctoral dissertation (article-based)
Abstract: Cell lysis, as a consequence of adverse conditions, has been recognized as an important loss process among phytoplankton, in addition to the well-known loss processes of grazing and sinking. Cell lysis has been connected to increased release of carbon fixed by phytoplankton as dissolved organic carbon (DOC), the primary carbon source for pelagic heterotrophic bacteria. This has the potential to enhance pelagic remineralization at the cost of reduced sedimentation of organic carbon. Cell lysis may, therefore, have global consequences as the ratio of pelagic remineralization to sedimentation widely determines whether oceans function as a source or a sink of atmospheric carbon. However, the subject has been studied predominantly in oceans and oligotrophic marine regions. The Baltic Sea is different from these environments and the causes and consequences of phytoplankton cell lysis may, therefore, be expected to differ. The studies included in this thesis are the first attempt to study phytoplankton cell lysis and its effect on carbon cycling in the Baltic Sea. The focus of the thesis is mainly on elucidating the abiotic and biological controls of cell lysis and its relationship with pelagic DOC concentration. These were studied on a spatial scale during a spring bloom on an area covering the Gulf of Finland, the Åland Sea and the Baltic Proper, and on a temporal scale during a two-year long monitoring campaign in an estuary in the northern Gulf of Finland. In both studies the proportion of cells undergoing lysis was measured using a membrane impermeable nucleic acid stain to indicate cells with compromised membrane integrity. The spatial monitoring study revealed considerable variation in the proportion of cells undergoing lysis with generally higher proportion of dying cells in deep water (1-10 m: average 84%, range 67-91%; 30 m: average 77%, range 62-90%; 60 m: average 71%, range 58-86%) and among nanophytoplankton (surface water average: 64%), as compared to smaller eukaryotic picophytoplankton (surface water average: 88%) and picocyanobacteria (surface water average: 82%). No clear correlations between cell lysis and nutrient concentrations were found, although there was a weak correlation between the proportion of intact eukaryotic picophytoplankton and phosphate concentration (R2 = 0.13, p = 0.029). No connection between cell lysis and DOC concentration was found. Also during the temporal monitoring campaign variation of cells undergoing lysis was high (surface water average: 62%, range 18-97%). Again, no correlation between nutrient concentrations and cell lysis was found, although this time there was a weak negative relationship between the proportion of cells undergoing lysis and DOC concentration (R2 = 0.15, p = 0.0185). In both studies some indication was found that phytoplankton lysis is less prevalent in conditions where interspecific phytoplankton competition is low. Details of the flow of carbon from phytoplankton to pelagic heterotrophic bacteria was studied experimentally using two phytoplankton species (a dinoflagellate Apocalathium malmogiense and a cryptophyte Rhodomonas marina). Contrasting species specific differences were found in their ability to transfer carbon from the inorganic pool via DOC to bacterial biomass and in the composition of the emerging bacterial community. The smaller R. marina released more bioavailable DOC and attracted a bacterial community mainly consisting of copiotrophs (bacteria thriving when DOC is abundant and highly bioavailable), which likely directs more carbon towards microbial loop. The DOC released by the larger A. malmogiense was less bioavailable. If these results can be generalized to other taxa of similar size, the fast consumption of DOC released by R. marina may partially explain why no relationship between the lysis of small phytoplankton and DOC concentration was found. The overarching conclusion from the two field studies is that the environmental conditions, such as nutrient limitation, that have been shown to promote cell lysis in oligotrophic marine regions are not the main determinants of cell lysis in the Baltic Sea. Also, the high ambient DOC concentration and terrestrial runoff in the Baltic Sea seem to mask the effect of cell lysis on DOC concentration. The group and species specific differences in both cell lysis and carbon cycling indicate that investigating cell lysis on lower taxonomic levels will help to connect cell lysis to carbon cycling.Kasviplanktonin yhteyttämisessään sitoma hiili siirtyy eteenpäin kasviplanktonsolujen upotessa, tullessa syödyksi tai hajotessa. Uppoaminen kuljettaa hiiltä vesipatsaan tuottavasta pintakerroksesta syvempiin vesikerroksiin ja meren pohjan eliöstölle, ja mahdollisesti poistaa hiiltä pinnan hiilenkierrosta pitkäksi aikaa. Eläinplanktonin laidunnus siirtää hiiltä suuremmille eläimille pinnan ravintoverkossa. Kasviplanktonsolujen hajoamisen vaikutusta hiilen kiertoon on tutkittu kahta muuta kuolleisuusmekanismia vähemmän eikä sen kaikkia seurauksia tiedetä. Väitöskirjassani selvitin hajoavien kasviplanktonsolujen osuutta kasviplanktonyhteisössä sekä kuolevien solujen vaikutusta erityisesti vesipatsaan liuenneen orgaanisen aineen määrään avoimella Itämerellä kevätkukinnan aikana sekä kahden vuoden seurannalla Suomenlahden pohjoisrannikolla. Selvitin myös ympäristön olosuhteiden vaikutusta kuolevien kasviplanktonsolujen osuuteen. Kenttätutkimusten lisäksi tutkin kokeellisesti kasviplanktonista lähtöisin olevan orgaanisen aineen käyttöä vesipatsaan bakteerien toimesta. Hajoavien solujen osuus oli alimmillaan 18% ja korkeimmillaan 97%. Toisin kuin valtamerissä, alhaiset ravinnepitoisuudet eivät selittäneet vaihtelua hajoavien solujen osuudessa Itämerellä. Hajoavia soluja oli vähiten silloin, kun kasviplanktonyhteisö koostui lähinnä yhdestä lajista, mikä voi viitata haitallisiin lajienvälisiin vuorovaikutuksiin yhtenä solujen hajoamista edistävänä tekijänä. Hajoavien kasviplanktonsolujen vuosittainen vaihtelu korreloi hieman liuenneen orgaanisen aineen pitoisuuden kanssa. Hajoavien kasviplanktonien määrällistä vaikutusta orgaanisen aineen kiertoon ei kuitenkaan pystytty määrittämään. Kokeissa havaittiin eroja eri kasviplanktonlajien tuottaman orgaanisen aineen määrässä ja laadussa sekä sen hajotuksessa ja sitä käyttävän mikrobiyhteisön koostumuksessa. Itämeren korkea liuenneen orgaanisen aineen määrä ja tuoreen orgaanisen aineen nopea hajotus bakteerien toimesta todennäköisesti selittävät, miksi valtamerissä havaittua yhteyttä liuenneen orgaanisen aineen pitoisuuksissa ja kasviplanktonin hajoamisessa ei havaittu Itämerellä yhtä selkeästi. Jotta Itämeren kasviplanktonin eri kuolleisuusmekanismien tarkka vaikutus hiilen kiertoon pystyttäisiin määrittämään, erot tärkeimpien kasviplanktonlajien tuottamassa liuenneessa orgaanisessa aineessa ja sen hajotuksessa tulisi tuntea paremmin.
Subject: biologia
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