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A Phytoplankton Invasion: Population Genetics, Phylogeography, and Invasion Success of Gonyostomum semen

Lebret, Karen LU (2012)
Abstract
nvasive species is a major threat to ecosystems and biodiversity. Invasions by macroorganisms have been intensively studied, but little is known concerning microbial invasions. In aquatic environments, phytoplankton, i.e. autotrophic microbes, have a key role as primary producers. In my thesis, I focused on the population genetic structure and phylogeography of the freshwater raphidophyte Gonyostomum semen, which is nowadays considered invasive in Northern Europe, as it has increased in abundance and occurence during the last decades.

Phytoplankton blooms were for a long time believed to be monoclonal, however recent studies have shown that phytoplankton blooms are highly diverse. G. semen can form blooms in lakes for extended... (More)
nvasive species is a major threat to ecosystems and biodiversity. Invasions by macroorganisms have been intensively studied, but little is known concerning microbial invasions. In aquatic environments, phytoplankton, i.e. autotrophic microbes, have a key role as primary producers. In my thesis, I focused on the population genetic structure and phylogeography of the freshwater raphidophyte Gonyostomum semen, which is nowadays considered invasive in Northern Europe, as it has increased in abundance and occurence during the last decades.

Phytoplankton blooms were for a long time believed to be monoclonal, however recent studies have shown that phytoplankton blooms are highly diverse. G. semen can form blooms in lakes for extended periods of time. In the first study, I investigated the population genetic structure and genetic diversity of G. semen in one lake over time, covering the different stages of the bloom using Amplified Fragment Lenght Polymorphism (AFLP). The genetic diversity of G. semen increased over time, especially at the beginning of the bloom. This increase was likely due to the recruitment of cysts from the sediment bringing new genotypes to the population. The blooms from two consecutive years formed a single genetic population, although a significant differentiation was detected. The results of this study highlight the importance of life cycle characteristics for the intraspecific genetic diversity of partially asexual organisms.

In the second study, I investigated the population genetic structure of G. semen in 11 lakes in Northern Europe using AFLP. I found that all the strains isolated from 11 lakes belong to a single genetic population, although significant differentiation was dectected between the sampling locations. The differentiation between locations was likely caused by founder effect following the colonization of the lakes. In addition, low genetic diversity was measured at each location, which could reflect the recent establishment of G. semen in the lakes. These results suggest that the colonization of G. semen in these lakes is relatively recent, and that G. semen has colonized new lakes. In addition, I performed a phylogeographic analysis with strains from 15 Northern European lakes, and two Japanese strains, by sequencing four DNA regions. All the strains from Northern Europe have identical sequences for the four markers. For one marker, the mitochondrial gene cox1, clear differences were detected between the sequences of the Japanese strains and the Northern European ones. In this study the low diversity observed in Northern Europe also support the hypothesis of recent expansion of G. semen. The results of these two studies are coherent with monitoring data suggesting recent invasion of new lakes by G. semen in Northern Europe.

Several factors can potentially facilitate the invasion by a species. The absence of a grazer for instance might facilitate the formation of a dense population of an invader. In G. semen, due to its large cell size and mucilage production, the grazing pressure was expected to be low. I performed grazing experiments to determine which potential grazers could feed on G. semen. I found that only the large cladoceran Daphnia magna was able to feed on G. semen. The large cell size of G. semen was likely limiting the grazing by smaller cladocerans, furtermore the mucilage production and expulsion of trichocsyts were likely limiting the feeding of copepods. Field data revealed that the large cladoceran D. magna do not co-exist in G. semen lakes. Thus the grazing pressure on G. semen is likely restricted, allowing the formation of dense populations, and potentially the establishment after colonization of new lakes. (Less)
Abstract (Swedish)
Popular Abstract in French

Phytoplancton invasif : génétique des populations, phylogéographie, et facteurs facilitant l’invasion par Gonyostomum semen

De nos jours, les espèces invasives représentent une importante menace à la biodiversité. Une espèce invasive colonise un nouvel environnement, ou elle était absente, et atteint de forte densité rapidement, diminuant l’abondance ou remplaçant les espèces natives. Chaque année, des dizaines de nouvelles espèces invasives sont détectées mondialement. La majorité des espèces qualifiées d’invasives sont des plantes ou des animaux. Par leur petite taille, les microorganismes (bactéries, protistes, ou champignons) sont difficiles à détecter dans l’environnement, donc très... (More)
Popular Abstract in French

Phytoplancton invasif : génétique des populations, phylogéographie, et facteurs facilitant l’invasion par Gonyostomum semen

De nos jours, les espèces invasives représentent une importante menace à la biodiversité. Une espèce invasive colonise un nouvel environnement, ou elle était absente, et atteint de forte densité rapidement, diminuant l’abondance ou remplaçant les espèces natives. Chaque année, des dizaines de nouvelles espèces invasives sont détectées mondialement. La majorité des espèces qualifiées d’invasives sont des plantes ou des animaux. Par leur petite taille, les microorganismes (bactéries, protistes, ou champignons) sont difficiles à détecter dans l’environnement, donc très peu de microorganismes sont qualifiés d’invasifs.

Dans les océans, lacs ou rivières, le phytoplancton, composé d’algues microscopiques, représente une partie importante de l’écosystème, étant à la base de la chaine alimentaire. Plusieurs espèces phytoplanctoniques produisent des composés toxiques qui peuvent induire d’importante mortalité de poissons, ou s’accumule dans la chair des fruits de mers et potentiellement toxiques pour l’homme en cas d’ingestion. Les algues peuvent aussi former de denses populations, appelées blooms, qui réduisent significativement la concentration d’oxygène dans l’eau quant les cellules du bloom meurent. Le manque d’oxygène peut être extrêmement nocif pour l’écosystème et induire la mort de poissons par exemple. Aujourd’hui, très peu d’espèces phytoplanctoniques sont qualifiées d’invasives. En Scandinavie et Finlande, l’algue microscopique Gonyostomum semen est suspectée d’avoir envahi de nombreux lacs. L’occurrence et abondance de cette espèce ont augmenté fortement durant les trois dernières décennies.

Les populations de phytoplancton peuvent être considérées comme étant éphémère, car les espèces peuvent former des blooms durant quelques semaines et disparaître de la colonne d’eau. La majorité des algues microscopiques peuvent former des cystes quant les conditions extérieures deviennent défavorables pour la croissance (par exemple pendant l’hiver), et attendre de meilleures conditions. Ces cystes peuvent survivre plusieurs années dans les sédiments avant de germer et former les cellules planctoniques. Dans cette thèse, j’ai étudié la structure génétique des populations de Gonyostomum de deux différents blooms. Les cellules de Gonyostomum isolées de deux blooms consécutifs appartenaient à la même population génétique, avec une légère différentiation entre les deux blooms. Cette différentiation a put être le résultat de la germination de cystes formés durant les précédentes années. Alternativement, différentes conditions environnementales ont pu déclencher la germination de différents cystes.

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L’étude de la structure génétique des populations a l’échelle géographique peut être utile pour comprendre comment une espèce est dispersée, migre, ou identifier la source d’une population. Dans, cette thèse, mes résultats montrent que Gonyostomum forment une seule population génétique en Suède, Finlande et Norvège, de plus la diversité génétique dans chaque lacs était faible. Ces résultats sont cohérents avec l’hypothèse que Gonyostomum a envahi les lacs durant les dernières décennies. Si Gonyostomum était déjà présent dans les lacs (depuis la dernière période glaciaire), les lacs du nord et du sud formeraient des populations différentes, après la colonisation progressive des lacs. De plus, la faible diversité détectée pour chaque lacs (avec l’utilisation d’une méthode de génétiques des populations et séquençage de spécifiques régions de l’ADN) peut être causé par la récente colonisation par quelques individus.

La réussite d’une invasion peut être influencé par différents facteurs. Par exemple, l’absence d’herbivores peut faciliter l’établissement et la formation de denses populations par une espèce invasive. Dans cette thèse, j’ai démontré que seul le zooplancton de grande taille peut manger Gonyostomum. La grande taille et la production de mucilage par Gonyostomum ont limité l’ingestion par les autres espèces de zooplancton. De plus, des données sur la composition du zooplancton et phytoplancton de plusieurs lacs suggèrent que les espèces de zooplancton de grande taille ne sont pas présentes dans les lacs ou Gonyostomum existe. L’absence d’herbivores pouvant manger Gonyostomum, peut potentiellement faciliter la formation de denses populations et donc envahir les lacs. (Less)
Please use this url to cite or link to this publication:
author
supervisor
opponent
  • Rynearson, Tatiana, Graduate School of Oceanography, University of Rhode Island, United States
organization
publishing date
type
Thesis
publication status
published
subject
pages
106 pages
publisher
Department of Biology, Lund University
defense location
Blue Hall, Ecology Building, Sölvegatan 37, Lund
defense date
2012-12-06 09:30:00
ISBN
978-91-7473-395-2
language
English
LU publication?
yes
id
8b49bac3-3432-4de6-8d12-fc467067fcff (old id 3166046)
date added to LUP
2016-04-04 10:25:35
date last changed
2018-11-21 20:58:41
@phdthesis{8b49bac3-3432-4de6-8d12-fc467067fcff,
  abstract     = {{nvasive species is a major threat to ecosystems and biodiversity. Invasions by macroorganisms have been intensively studied, but little is known concerning microbial invasions. In aquatic environments, phytoplankton, i.e. autotrophic microbes, have a key role as primary producers. In my thesis, I focused on the population genetic structure and phylogeography of the freshwater raphidophyte Gonyostomum semen, which is nowadays considered invasive in Northern Europe, as it has increased in abundance and occurence during the last decades.<br/><br>
Phytoplankton blooms were for a long time believed to be monoclonal, however recent studies have shown that phytoplankton blooms are highly diverse. G. semen can form blooms in lakes for extended periods of time. In the first study, I investigated the population genetic structure and genetic diversity of G. semen in one lake over time, covering the different stages of the bloom using Amplified Fragment Lenght Polymorphism (AFLP). The genetic diversity of G. semen increased over time, especially at the beginning of the bloom. This increase was likely due to the recruitment of cysts from the sediment bringing new genotypes to the population. The blooms from two consecutive years formed a single genetic population, although a significant differentiation was detected. The results of this study highlight the importance of life cycle characteristics for the intraspecific genetic diversity of partially asexual organisms.<br/><br>
In the second study, I investigated the population genetic structure of G. semen in 11 lakes in Northern Europe using AFLP. I found that all the strains isolated from 11 lakes belong to a single genetic population, although significant differentiation was dectected between the sampling locations. The differentiation between locations was likely caused by founder effect following the colonization of the lakes. In addition, low genetic diversity was measured at each location, which could reflect the recent establishment of G. semen in the lakes. These results suggest that the colonization of G. semen in these lakes is relatively recent, and that G. semen has colonized new lakes. In addition, I performed a phylogeographic analysis with strains from 15 Northern European lakes, and two Japanese strains, by sequencing four DNA regions. All the strains from Northern Europe have identical sequences for the four markers. For one marker, the mitochondrial gene cox1, clear differences were detected between the sequences of the Japanese strains and the Northern European ones. In this study the low diversity observed in Northern Europe also support the hypothesis of recent expansion of G. semen. The results of these two studies are coherent with monitoring data suggesting recent invasion of new lakes by G. semen in Northern Europe.<br/><br>
Several factors can potentially facilitate the invasion by a species. The absence of a grazer for instance might facilitate the formation of a dense population of an invader. In G. semen, due to its large cell size and mucilage production, the grazing pressure was expected to be low. I performed grazing experiments to determine which potential grazers could feed on G. semen. I found that only the large cladoceran Daphnia magna was able to feed on G. semen. The large cell size of G. semen was likely limiting the grazing by smaller cladocerans, furtermore the mucilage production and expulsion of trichocsyts were likely limiting the feeding of copepods. Field data revealed that the large cladoceran D. magna do not co-exist in G. semen lakes. Thus the grazing pressure on G. semen is likely restricted, allowing the formation of dense populations, and potentially the establishment after colonization of new lakes.}},
  author       = {{Lebret, Karen}},
  isbn         = {{978-91-7473-395-2}},
  language     = {{eng}},
  publisher    = {{Department of Biology, Lund University}},
  school       = {{Lund University}},
  title        = {{A Phytoplankton Invasion: Population Genetics, Phylogeography, and Invasion Success of Gonyostomum semen}},
  year         = {{2012}},
}