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Structure and dynamics of the zooplankton symbiotic microbiome
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.ORCID iD: 0000-0002-6392-728X
2025 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Zooplankton is a key group of organisms in aquatic ecosystems that regulate element cycling, transport carbon and energy between trophic levels, and stabilize aquatic community structure. Their ecological importance is further emphasized by the fact that zooplankton are also microbial hotspots for diverse prokaryotic and eukaryotic microbes. The association between zooplankton and the microbes ranges from beneficial symbiotic to harmful parasitic interactions. Symbiotic associations contribute to multiple ecological functions, such as enhanced nutrient recycling, adaptation to unfavourable conditions and combating stresses, while parasitic interactions reduce species fecundity and increase mortality. Hence, the association between zooplankton and their microbes contributes to the structure and functioning of aquatic ecosystems. However, the dynamics of zooplankton-associated prokaryotic and eukaryotic organisms is largely unknown. 

In this study, the diversity, dynamics and drivers of the zooplankton symbiotic and parasitic communities were studied across the Baltic Sea environmental gradients to increase understanding about their ecological roles in aquatic ecosystems. The zooplankton associated microbial community composition was revealed by DNA metabarcoding, statistical modelling and machine learning. The communities were examined from different angles: taxonomic composition, functional clustering and phylogenetic structure. In Chapters I and IV of this thesis, the dynamics of zooplankton-associated symbiotic prokaryotes and parasitic eukaryotes were elucidated from the perspective of taxonomic composition, which were observed to fluctuate with environmental gradients and showed some host-specificity. Diet diversity and composition, and the ecological niche of the host contributed to the dynamics of zooplankton-associated microbial communities. In Chapter II, by focusing on bacterial communities associated with zooplankton, functional grouping of different bacterial taxa increased the explained variance of the symbiotic community structure. The mismatch between the bacterial functionality grouping and host or environmental gradients emphasized the general influence of environmental parameters, such as temperature and phosphorus, and more specific effects of host diet composition on gut bacterial communities. Chapter III investigated dynamic patterns of zooplankton microbiome identified by phylogenetic structure, in addition to the observed taxonomic and functional variation. The distribution of phylogenetically clustered and divergent communities was highly location-specific, implying the importance of background bacteria to symbiotic communities. Besides the abundant bacteria, the contribution of less abundant bacteria to the structure of the communities was significant, suggesting that the entire bacterial community needs to be considered to understand the dynamics and functions of the microbiome. 

This thesis reveals that zooplankton-associated microbial communities are subject to both environmental factors and host feeding behaviour, and that the gut bacterial functionality contributes to the zooplanktons’ adaptation capacity to different environmental conditions.  Focusing on the symbionts’ functionality and phylogeny, rather than taxonomic composition, improves our understanding of the microbiome dynamics. This thesis provides inspiration to further map symbiotic communities at large ecological scales and advances our understanding of the species diversity and potential functionality hidden inside organisms. 

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University , 2025. , p. 62
Keywords [en]
zooplankton, symbiotic prokaryotes, parasitic eukaryotes, community dynamics
National Category
Ecology
Research subject
Marine Biology
Identifiers
URN: urn:nbn:se:su:diva-241958ISBN: 978-91-8107-246-4 (print)ISBN: 978-91-8107-247-1 (electronic)OAI: oai:DiVA.org:su-241958DiVA, id: diva2:1951733
Public defence
2025-06-05, Vivi Täckholmsalen lecture hall, house NPQ, Svante Arrhenius väg 20 A, Stockholm, 13:30 (English)
Opponent
Supervisors
Available from: 2025-05-13 Created: 2025-04-13 Last updated: 2025-04-29Bibliographically approved
List of papers
1. Dynamics of Gut Bacteria Across Different Zooplankton Genera in the Baltic Sea
Open this publication in new window or tab >>Dynamics of Gut Bacteria Across Different Zooplankton Genera in the Baltic Sea
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2024 (English)In: Microbial Ecology, ISSN 0095-3628, E-ISSN 1432-184X, Vol. 87, no 1, article id 48Article in journal (Refereed) Published
Abstract [en]

In aquatic ecosystems, zooplankton-associated bacteria potentially have a great impact on the structure of ecosystems and trophic networks by providing various metabolic pathways and altering the ecological niche of host species. To understand the composition and drivers of zooplankton gut microbiota, we investigated the associated microbial communities of four zooplankton genera from different seasons in the Baltic Sea using the 16S rRNA gene. Among the 143 ASVs (amplified sequence variants) observed belonging to heterotrophic bacteria, 28 ASVs were shared across all zooplankton hosts over the season, and these shared core ASVs represented more than 25% and up to 60% of relative abundance in zooplankton hosts but were present at low relative abundance in the filtered water. Zooplankton host identity had stronger effects on bacterial composition than seasonal variation, with the composition of gut bacterial communities showing host-specific clustering patterns. Although bacterial compositions and dominating core bacteria were different between zooplankton hosts, higher gut bacteria diversity and more bacteria contributing to the temporal variation were found in Temora and Pseudocalanus, compared to Acartia and Synchaeta. Diet diatom and filamentous cyanobacteria negatively correlated with gut bacteria diversity, but the difference in diet composition did not explain the dissimilarity of gut bacteria composition, suggesting a general effect of diet on the inner conditions in the zooplankton gut. Synchaeta maintained high stability of gut bacterial communities with unexpectedly low bacteria-bacteria interactions as compared to the copepods, indicating host-specific regulation traits. Our results suggest that the patterns of gut bacteria dynamics are host-specific and the variability of gut bacteria is not only related to host taxonomy but also related to host behavior and life history traits.

Keywords
Diet effects, Gut microbiome, Host specificity, Temporal variability, Zooplankton
National Category
Ecology Microbiology
Identifiers
urn:nbn:se:su:diva-235490 (URN)10.1007/s00248-024-02362-7 (DOI)001172870200001 ()2-s2.0-85186257832 (Scopus ID)
Available from: 2024-11-15 Created: 2024-11-15 Last updated: 2025-04-13Bibliographically approved
2. Functional bacterial clusters describe the spatiotemporal variation of the zooplankton microbiomes
Open this publication in new window or tab >>Functional bacterial clusters describe the spatiotemporal variation of the zooplankton microbiomes
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

 Zooplankton and bacteria are two critical groups of aquatic organisms and their associations play important roles in contributing to ecological processes. However, the taxonomy patterns and dynamics of zooplankton-associated bacterial communities across different hosts over temporal and spatial gradients are seldom described in nature[KJ1] . Here, 16s rRNA sequencing and functional annotation were implemented on the bacterial communities of 12 zooplankton genera sampled across the Baltic Sea salinity gradient in two seasons. Our results suggest that functional grouping of the zooplankton-associated bacteria captures host and environment specific patterns better than bacteria taxonomic composition. The distribution of functional clusters of bacteria identified by K-medoid did not strictly follow host taxonomy, temporal and spatial gradients. But certain clusters, such as clusters of higher potential for unsaturated fatty acid synthesis showed host and temporal specificity. These specificities were further analyzed by random forest, suggesting that the dynamics of zooplankton-associated bacteria were related to environmental parameters such as temperature and phosphorus, and host diet composition. These results implied the co-effects of abiotic factors and biotic host lifestyles shaping the dynamics of zooplankton bacterial communities.

Keywords
Zooplankton, Gut bacteria, Functional clustering, Spatiotemporal variation
National Category
Ecology
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-241984 (URN)
Available from: 2025-04-11 Created: 2025-04-11 Last updated: 2025-04-13
3. Phylogenetically clustered and divergent zooplankton gut bacteria distribute along environmental and diet gradients
Open this publication in new window or tab >>Phylogenetically clustered and divergent zooplankton gut bacteria distribute along environmental and diet gradients
(English)Manuscript (preprint) (Other academic)
Abstract [en]

The association of zooplankton and bacteria provides benefits to both groups of organisms and their symbiotic relation performs important ecological functions. The temporal, spatial and host-specific patterns of zooplankton gut bacterial communities is largely explained with shifts in dominating bacteria and alpha diversity. Due to hypothesized unique evolutionary history for adapting symbiotic life, gut bacterial communities can show distinct phylogenetic structures whose general patterns across hosts and environments remain unclear. Here we describe the gut bacterial communities associated to zooplankton from the perspective of bacteria phylogenetic relatedness and relative abundance. Our results suggest both phylogenetically close and distant related bacterial communities existed in zooplankton gut, termed clustered and divergent communities respectively. Their distribution shows spatial specificity across sampling locations and thus environmental conditions. For clustered bacterial communities, abundant bacteria contributed to the phylogenetic structure more than less abundant bacteria, while an opposite result observed for divergent communities. The difference between more abundant and less abundant bacteria contribution correlated with physical environmental factors, temperature and salinity. Diet evenness of host was more important to gut bacteria communities than host taxa and dominating bacteria in the gut. These results suggest that environment and feeding behavior affect the phylogenetic structures of zooplankton gut bacterial communities.

Keywords
Zooplankton, Gut bacteria, Community phylogenetic structure, diet
National Category
Ecology
Research subject
Marine Ecology; Marine and Brackish Water Ecology
Identifiers
urn:nbn:se:su:diva-241987 (URN)
Available from: 2025-04-11 Created: 2025-04-11 Last updated: 2025-04-13
4. Protist parasitic Syndiniales show host-specificity in crustacean zooplankton
Open this publication in new window or tab >>Protist parasitic Syndiniales show host-specificity in crustacean zooplankton
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

 The marine alveolates consist of a group of protist parasitic dinoflagellates belonging to the order Syndiniales, which infect other planktonic taxa, including other dinoflagellates, copepods, and cladocerans. The ecological roles of Syndiniales linked to zooplankton remain poorly understood, though some Syndiniales Groups (SGs) are known to consistently kill their hosts. We identified the associated Syndiniales-zooplankton interactions of selected taxa using DNA metabarcoding across the environmental gradient of the Baltic Sea. We determined the abiotic drivers of these interactions and the infection pathways through the prey consumed by the hosts. We found variations in Amplicon Sequence Variants (ASVs) of different Syndiniales groups associated with zooplankton. The Syndiniales associations with zooplankton were driven highly by low-oxygen water conditions. The environmental variables create unique niches for both the hosts and the parasites, driving niche-specific associations. These interactions demonstrate species specificity shaped by host feeding behaviour and the surrounding abiotic environments. These findings indicate that niche-specific interactions occur along the environmental gradients of the Baltic Sea.

Keywords
Zooplankton, Syndiniales, host-specificity
National Category
Ecology
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-241990 (URN)
Available from: 2025-04-11 Created: 2025-04-11 Last updated: 2025-04-13

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