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Organic Contaminant Mixture Significantly Changes Microbenthic Community Structure and Increases the Expression of PAH Degradation Genes
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
Stockholm University, Faculty of Science, Department of Environmental Science.ORCID iD: 0000-0002-3399-1483
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. University of Southern Denmark, Denmark; University of Gothenburg, Sweden.ORCID iD: 0000-0003-4366-0677
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences. Stockholm University, Faculty of Science, Stockholm University Baltic Sea Centre.
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Number of Authors: 62020 (English)In: Frontiers in Environmental Science, E-ISSN 2296-665X, Vol. 8, article id 128Article in journal (Refereed) Published
Abstract [en]

Studying the effects of chemical contaminants on the structure and function of microbial and meiofauna communities have traditionally focused on specific effects of single contaminants on single species. This has left the complex interactions between mixtures of contaminants and its non-specific toxicity effects on the functions and structure of sediment microbial communities mostly overlooked. In order to improve our insights on such questions, we performed an experiment where Baltic Sea sediments were spiked with an ecologically relevant mixture of seven organic contaminants below specific toxicity levels and used 16S and 18S rRNA metabarcoding from RNA extracts to monitor changes in active microbial and meiofauna diversity and community structure in the spiked treatment compared to controls. In addition, we investigated the effects of exposure to this contaminant mixture on potential nitrification rates and on the expression of key-genes in the microbial nitrification and PAH degradation pathways with qPCR. There were significant differences in both eukaryotic and microbial community structures in sediments spiked with a mixture of organic contaminants. Nematoda showed a significant increase in overall relative abundance to the added contaminants (5.5 ± 1.1% higher in spiked), particularly taxa of the genus Leptolaimus (increased from 10.2 ± 5.4% in the controls to 32.5 ± 10.2% in the spiked treatment). Conversely, a significant decrease in relative abundance from 18.2 ± 5.6% in control to 7 ± 3.4% in of the genus Paraplectana was also detected. Additionally, while the abundance of active PAH degraders was significantly higher in spiked sediments than in the controls, no significant effect of our organic mixture was found on nitrification rates or the expression of AmoA (bacterial ammonia oxidizer gene). Our data indicate that mixtures of organic contaminants can have significant effects on microbenthic community structure even when its individual components are present at concentrations below its specific toxicity. In addition, we suggest that eRNA-based metabarcoding can offer important insights in microbenthic community structure and activities, and further empathizes the potential of meiofauna as bio-indicators of chemical contamination in benthic ecosystems.

Place, publisher, year, edition, pages
2020. Vol. 8, article id 128
Keywords [en]
non-specific toxicity, meiobenthos, microbial, metabarcoding, polychlorinated biphenyl, polycyclic aromatic hydrocarbons
National Category
Earth and Related Environmental Sciences
Identifiers
URN: urn:nbn:se:su:diva-186669DOI: 10.3389/fenvs.2020.00128ISI: 000566221800001OAI: oai:DiVA.org:su-186669DiVA, id: diva2:1502539
Available from: 2020-11-20 Created: 2020-11-20 Last updated: 2025-02-07Bibliographically approved
In thesis
1. Microbenthos under Pressure: Impacts of human activities on bacteria and meiofauna communities in Baltic soft sediments
Open this publication in new window or tab >>Microbenthos under Pressure: Impacts of human activities on bacteria and meiofauna communities in Baltic soft sediments
2022 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The marine benthic zone is one of the largest habitats on the planet, harbouring a large diversity of life that underpin many important ecological processes. However, these habitats have been under growing stress from human activities, profoundly altering their living communities. How microbial communities respond to various anthropogenic disturbances has been a central topic in ecology, but the response of meiofauna (benthic microeukaryotes, 40 µm ≥ 1 mm in size) and their use as potential bioindicators in a whole-community approach, has received less attention. The Baltic Sea has been of particular interest in studying how ecological processes are affected due to its history and continuous exposure to various anthropogenic stresses. In this thesis, I explored the effects of chemical contamination (Study I), recreational boating activity (Study II), bottom trawling fishing (Study III), and hypoxia (Study IV) on the Baltic microbenthos in terms of structure and diversity using DNA-inferred community analysis in the context of controlled experiments (Studies I and IV) and field studies (Studies II and III). Study I showed a clear increase in contaminated sediments in PAH degradation, relative abundance of Pseudomonas amongst bacteria, and nematodes amongst meiofauna. Study IV showed that high meiofauna abundance, and its bioturbation, altered sediment oxygen penetration and sulphide oxidation in hypoxic conditions with clear effects on bacterial community structure. Studies II and III showed that select bacteria and meiofauna taxa were favoured in areas with high levels of disturbance. In Study II, the ostracod family Cypridoidea was found in higher abundance in bays with high recreational boating activity (marinas) whilst Cytheruridae was significantly lower. Amongst bacteria, Burkholderiaceae showed to be favoured in active marinas and served as an indicator of chemical contamination. In Study III, highly trawled areas appeared to favour Rhabdocoels flatworms and were accompanied by a decrease in Rhizobiales amongst bacteria, suggesting improved feeding opportunities for motile flatworms, and a negative pressure on substrate dependent bacteria. However, the exposure to the open sea was a major factor in structuring both meiofauna and bacterial communities in shallow bays (Study II) and the impact of trawling (Study III) was more pronounced between areas that were geographically closer. This highlights the importance of abiotic and location specific co-factors that drive microbial and meiofauna assemblages and stress the impact of survey design and sampling locations. Additionally, a common trend throughout my work emphasised the potential of select microbial taxa as bioindicators. For example, the bacteria families Pseudomonadaceae and Burkholderiaceae, and the nematode genera Sabatieria and Leptolaimus could be used as bacterial and meiofauna bioindicators of chemical contamination. In brief, chemical stress had a significant effect on bacterial community structure, whereas physical disturbances had a more pronounced effect on meiofauna, both in terms of structural changes as well as alpha diversity. As such, combining the study of meiofauna and microbial assemblages could be a useful approach in assessing the effects of a wide range of disturbances in benthic habitats.

Abstract [sv]

Den marina bentiska regionen täcker en stor del av jordens yta och är en av de största miljöerna med liv på planeten. Här finns en stor diversitet av liv. Kuster och grunda ekosystem står för stor del av ekologiska processer och deras biologiska samhällen spelar en viktig roll i att flytta energi från sjöbotten till andra närliggande ekosystem. Men marina livsmiljöer har blivit påverkade av en mängd mänskliga aktiviteter. Detta har förändrat akvatiska organismers samhällen och ekologiska processer, samt näringskedjor som dessa möjliggör. I dessa ekosystem utgör mikroorganismer och meiofauna (små bentiska djur <1 mm) ofta en viktig roll. Att studera hur mikrobiologiska samhällen påverkas av olika antropogeniska variabler har varit en central strävan i ekologi, men påverkan på meiofauna och dess roll som potentiella bioindikatorer har studerats mindre. I denna avhandling har jag studerat vilken effekt olika miljöpåverkande faktorer har på mikrobiologiska och meiofauna samhällen. På grund av exponering för en uppsjö antropogeniska föroreningar har bentiska livsmiljöer i Östersjön varit av extra intresse för att studera hur ekologiska processor påverkas. I denna avhandling utforskade jag hur kemisk förorening (Studie I), fritidsbåtars aktivitet (Studie II), bottentrålning (Studie III) och syrebrist (Studie IV) påverkar bentiska mikroorganism- och meiofaunasamhällen i mjuka sediment. Övergripande så visade våra resultat att de undersökta antropogeniska stressfaktorerna hade en större effekt på sammansättningen av mikroorganismer och meiofauna än deras mångfald. När en hög variation av abiotiska medfaktorer kunde experimentellt kontrolleras (Studie I och IV) så observerade vi en tydligt omstruktureringen av mikrobiella- och meiofaunasamhällen, samt mikrobiell aktivitet. Studie I visade en tydlig ökning av nedbrytningen av PAH och den relativa mängden av Pseudomonas bland bakterierna, och nematoder i meiofaunasamhällen under kemisk stress. Studie IV visade att hög meiofaunamängd och bioturbation ändrade de biogeokemiska egenskaperna i sedimentet (syredjup och sulfidoxidation) under syrefattiga förhållanden med en tydlig effekt på den bakteriella samhällsstrukturen. Studie II och III återspeglade en liknande trend att specifika bakterier och meiofauna gynnades under förhållanden av stress, och hade en högre relativ abundans i områden med hög nivå av miljöstörande faktorer. I studie II så var ostrakodfamiljen Cypridoidea mer förekommande i aktiva småbåtshamnar, medan familjen Cytheruridae var signifikant mindre förekommande. I det bakteriella samhället så gynnades Burkholderiaceae i aktiva småbåtshamnar vilket kan ge en indikation av kemisk förorening. I studie III verkade plattmaskar tillhörande Rhabdocoels gynnas i de områden som hade hög aktivitet av trålning. I dessa områden minskade bakterierna Rhizobiales vilket indikerade på att dessa bakterier kunde vara en möjlig födokälla för plattmaskarna. I de grunda vikarna (Studie II) så var exponeringen till det öppna havet en huvudfaktor för struktureringen av både meiofauna och bakteriella samhällena. Effekten av trålning (Studie III) var mer tydligt mellan områden som var geografiskt nära varandra, vilket visar på betydelsen av abiotiska och lokalspecifika medfaktorer som drivande i mikrobiella och meiofaunasamhällen, samt betydelsen av studiedesign och provtagningsplatser. En förekommande trend genom detta arbete har varit betonandet av meiofauna som potentiella bioindikatorer. Till exempel så var bakterierna Pseudomonas och Burkholderiaceae samt nematoderna Sabatieria and Leptolaimus potentiella bakteriella och meiofauna bioindikatorer för kemisk förorening. Kemisk stress hade en signifikant effekt på den bakteriella samhällsstrukturen medan fysiska faktorer hade en tydligare effekt på mångfalden och strukturen av meiofauna. Kombinationen av studier om meiofauna och mikrobiella sammansättningar kan därför vara ett användbart verktyg för att bedöma effekterna av olika miljöstörande faktorer på bentiska livsmiljöer.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University, 2022. p. 70
Keywords
soft sediments, benthic ecosystems, anthropogenic disturbance, contamination, recreational boating, bottom trawling, meiofauna, bacteria, metabarcoding, Baltic Sea, mjuka sediment, bentiska ekosystem, antropogenisk påverkan, förorening, fritidsbåtar, bottentrålning, meiofauna, bakterier, metabarcoding, Östersjön
National Category
Ecology
Research subject
Marine Ecology
Identifiers
urn:nbn:se:su:diva-200276 (URN)978-91-7911-754-2 (ISBN)978-91-7911-755-9 (ISBN)
Public defence
2022-02-18, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 13:30 (English)
Opponent
Supervisors
Available from: 2022-01-26 Created: 2022-01-04 Last updated: 2022-01-21Bibliographically approved

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Iburg, SvenNybom, InnaBonaglia, StefanoKarlson, Agnes M. L.Sobek, AnnaNascimento, Francisco J. A.

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