Browsing by Author "Muyzer, Gerard"
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- Characterization and comparison of bacterial communities of an invasive and two native Caribbean seagrass species sheds light on the possible influence of the microbiome on invasive mechanismsPublication . Aires, Tania; Stuij, Tamara M.; Muyzer, Gerard; Serrao, Ester; Engelen, AschwinInvasive plants, including marine macrophytes, are one of the most important threats to biodiversity by displacing native species and organisms depending on them. Invasion success is dependent on interactions among living organisms, but their study has been mostly limited to negative interactions while positive interactions are mostly underlooked. Recent studies suggested that microorganisms associated with eukaryotic hosts may play a determinant role in the invasion process. Along with the knowledge of their structure, taxonomic composition, and potential functional profile, understanding how bacterial communities are associated with the invasive species and the threatened natives (species-specific/environmentally shaped/tissue-specific) can give us a holistic insight into the invasion mechanisms. Here, we aimed to compare the bacterial communities associated with leaves and roots of two native Caribbean seagrasses (Halodule wrightii and Thalassia testudinum) with those of the successful invader Halophila stipulacea, in the Caribbean island Curaçao, using 16S rRNA gene amplicon sequencing and functional prediction. Invasive seagrass microbiomes were more diverse and included three times more species-specific core OTUs than the natives. Associated bacterial communities were seagrass-specific, with higher similarities between natives than between invasive and native seagrasses for both communities associated with leaves and roots, despite their strong tissue differentiation. However, with a higher number of OTUs in common, the core community (i.e., OTUs occurring in at least 80% of the samples) of the native H. wrightii was more similar to that of the invader H. stipulacea than T. testudinum, which could reflect more similar essential needs (e.g., nutritional, adaptive, and physiological) between native and invasive, in contrast to the two natives that might share more environment-related OTUs. Relative to native seagrass species, the invasive H. stipulacea was enriched in halotolerant bacterial genera with plant growth-promoting properties (like Halomonas sp. and Lysinibacillus sp.) and other potential beneficial effects for hosts (e.g., heavy metal detoxifiers and quorum sensing inhibitors). Predicted functional profiles also revealed some advantageous traits on the invasive species such as detoxification pathways, protection against pathogens, and stress tolerance. Despite the predictive nature of our findings concerning the functional potential of the bacteria, this investigation provides novel and important insights into native vs. invasive seagrasses microbiome. We demonstrated that the bacterial community associated with the invasive seagrass H. stipulacea is different from native seagrasses, including some potentially beneficial bacteria, suggesting the importance of considering the microbiome dynamics as a possible and important influencing factor in the colonization of non-indigenous species. We suggest further comparison of H. stipulacea microbiome from its native range with that from both the Mediterranean and Caribbean habitats where this species has a contrasting invasion success. Also, our new findings open doors to a more in-depth investigation combining meta-omics with bacterial manipulation experiments in order to confirm any functional advantage in the microbiome of this invasive seagrass.
- Diversity of the holopelagic Sargassum microbiome from the Great Atlantic Sargassum Belt to coastal stranding locationsPublication . Theirlynck, Tom; Mendonça, Inara Regina W.; Engelen, Aschwin; Bolhuis, Henk; Collado-Vides, Ligia; van Tussenbroek, Brigitta I.; García-Sánchez, Marta; Zettler, Erik; Muyzer, Gerard; Amaral-Zettler, LindaThe holopelagic brown macroalgae Sargassum natans and Sargassum fluitans form essential habitats for attached and mobile fauna which contributes to a unique biodiversity in the Atlantic Ocean. However, holopelagic Sargassum natans (genotype I & VIII) and Sargassum fluitans (genotype III) have begun forming large accumu-lations with subsequent strandings on the western coast of Africa, the Caribbean and northern Brazil, threatening local biodiversity of coastal ecosystems and triggering economic losses. Moreover, stranded masses of hol-opelagic Sargassum may introduce or facilitate growth of bacteria that are not normally abundant in coastal regions where Sargassum is washing ashore. Hitherto, it is not clear how the holopelagic Sargassum microbiome varies across its growing biogeographic range and what factors drive the microbial composition. We determined the microbiome associated with holopelagic Sargassum from the Great Atlantic Sargassum Belt to coastal stranding sites in Mexico and Florida. We characterized the Sargassum microbiome via amplicon sequencing of the 16S V4 region hypervariable region of the rRNA gene. The microbial community of holopelagic Sargassum was mainly composed of photo(hetero)trophs, organic matter degraders and potentially pathogenic bacteria from the Pseudomonadaceae, Rhodobacteraceae and Vibrionaceae. Sargassum genotypes S. natans I, S. natans VIII and S. fluitans III contained similar microbial families, but relative abundances and diversity varied. LEfSE analyses further indicated biomarker genera that were indicative of Sargassum S. natans I/VIII and S. fluitans III. The holopelagic Sargassum microbiome showed biogeographic patterning with high relative abundances of Vibrio spp., but additional work is required to determine whether that represents health risks in coastal environments. Our study informs coastal management policy, where the adverse sanitary effects of stranded Sargassum might impact the health of coastal ecosystems.
- Draft genome of the marine bacterium alteromonas gracilis strain J4 isolated from the green coenocytic alga Caulerpa proliferaPublication . van Duijnhoven, Julia; Dombrowski, Nina; Kuperus, Peter; Aires, Tania; A. G. Coelho, Márcio; Silva, João; Muyzer, Gerard; Engelen, Aschwin; Frank J. StewartHere, we present the draft genome sequence of Alteromonas gracilis strain J4, isolated from the green macroalga Caulerpa prolifera. The draft genome is 4,492,914 bp in size and contains 4,719 coding DNA sequences, 67 tRNAs, and 16 rRNA-coding genes. Strain J4 may exhibit host growth-promoting properties.
- Impact of persistently high sea surface temperatures on the rhizobiomes of Zostera marina in a Baltic Sea benthocosmsPublication . Cúcio, Catarina; Brakel, Janina; Weinberger, Florian; Wahl, Martin; Teles, Ana; Muyzer, Gerard; Aires, Tania; Engelen, AschwinPersistently high marine temperatures are escalating and threating marine biodiversity. The Baltic Sea, warming faster than other seas, is a good model to study the impact of increasing sea surface temperatures. Zostera marina, a key player in the Baltic ecosystem, faces susceptibility to disturbances, especially under chronic high temperatures. Despite the increasing number of studies on the impact of global warming on seagrasses, little attention has been paid to the role of the holobiont. Using an outdoor benthocosm to replicate near-natural conditions, this study explores the repercussions of persistent warming on the microbiome of Z. marina and its implications for holobiont function. Results show that both seasonal warming and chronic warming, impact Z. marina roots and sediment microbiome. Compared with roots, sediments demonstrate higher diversity and stability throughout the study, but temperature effects manifest earlier in both compartments, possibly linked to premature Z. marina die-offs under chronic warming. Shifts in microbial composition, such as an increase in organic matter-degrading and sulfur-related bacteria, accompany chronic warming. A higher ratio of sulfate-reducing bacteria compared to sulfide oxidizers was found in the warming treatment which may result in the collapse of the seagrasses, due to toxic levels of sulfide. Differentiating predicted pathways for warmest temperatures were related to sulfur and nitrogen cycles, suggest an increase of the microbial metabolism, and possible seagrass protection strategies through the production of isoprene. These structural and compositional variations in the associated microbiome offer early insights into the ecological status of seagrasses. Certain taxa/genes/pathways may serve as markers for specific stresses. Monitoring programs should integrate this aspect to identify early indicators of seagrass health. Understanding microbiome changes under stress is crucial for the use of potential probiotic taxa to mitigate climate change effects. Broader-scale examination of seagrass-microorganism interactions is needed to leverage knowledge on host-microbe interactions in seagrasses.
- Metagenomic analysis shows the presence of bacteria related to free-living forms of sulfur-Oxidizing Chemolithoautotrophic Symbionts in the rhizosphere of the seagrass Zostera marinaPublication . Cúcio, Catarina; Overmars, Lex; Engelen, Aschwin; Muyzer, GerardSeagrasses play an important role as ecosystem engineers; they provide shelter to many animals and improve water quality by filtering out nutrients and by controlling pathogens. Moreover, their rhizosphere promotes a myriad of microbial interactions and processes, which are dominated by microorganisms involved in the sulfur cycle. This study provides a detailed insight into the metabolic sulfur pathways in the rhizobiome of the seagrass Zostera marina, a dominant seagrass species across the temperate northern hemisphere. Shotgun metagenomic sequencing revealed the relative dominance of Gamma- and Deltaproteobacteria, and comparative analysis of sulfur genes identified a higher abundance of genes related to sulfur oxidation than sulfate reduction. We retrieved four high-quality draft genomes that are closely related to the gill symbiont of the clam Solemya velum, which suggests the presence of putative free-living forms of symbiotic bacteria. These are potentially highly versatile chemolithoautotrophic bacteria, able to alternate their metabolism between parallel pathways of sulfide oxidation (via sqr and fcc), nitrate reduction (denitrification or DNRA) and carbon fixation (via CBB or TCA cycle), depending on the environmental availability of sulfide. Our results support the hypothesis that seagrass meadows might function as a source of symbionts for invertebrates that inhabit within or around seagrass meadows. While providing ideal conditions for the proliferation of these free-living forms of symbionts, seagrasses would benefit from their genetic versatility, which contributes to sulfide detoxification and ammonium production, the seagrasses' preferred nitrogen source.
- Rhizosphere microbiomes of european seagrasses are selected by the plant, but are not species specificPublication . Cucio, Catarina; Engelen, Aschwin H.; Costa, Rodrigo; Muyzer, GerardSeagrasses are marine flowering plants growing in soft-body sediments of intertidal and shallow sub-tidal zones. They play an important role in coastal ecosystems by stabilizing sediments, providing food and shelter for animals, and recycling nutrients. Like other plants, seagrasses live intimately with both beneficial and unfavorable microorganisms. Although much is known about the microbiomes of terrestrial plants, little is known about the microbiomes of seagrasses. Here we present the results of a detailed study on the rhizosphere microbiome of seagrass species across the North-eastern Atlantic Ocean: Zostera marina, Zostera noltii, and Cymodocea nodosa. High-resolution amplicon sequencing of 16S rRNA genes showed that the rhizobiomes were significantly different from the bacterial communities of surrounding bulk sediment and seawater. Although we found no significant differences between the rhizobiomes of different seagrass species within the same region, those of seagrasses in different geographical locations differed strongly. These results strongly suggest that the seagrass rhizobiomes are shaped by plant metabolism, but not coevolved with their host. The core rhizobiome of seagrasses includes mostly bacteria involved in the sulfur cycle, thereby highlighting the importance of sulfur-related processes in seagrass ecosystems.
- Seaweed loads cause stronger bacterial community shifts in coastal lagoon sediments than nutrient loadsPublication . Aires, Tânia; Muyzer, Gerard; Serrao, Ester; Engelen, AschwinThe input of nutrients from anthropogenic sources is the leading cause of coastal eutrophication and is usually coupled with algal/seaweed blooms. Effects may be magnified in semi-enclosed systems, such as highly productive coastal lagoon ecosystems. Eutrophication and seaweed blooms can lead to ecosystem disruption. Previous studies have considered only one of these factors, disregarding possible interactive effects and the effect of the blooming species' identity on sediment bacterial communities. We tested the effect of experimental nutrient loading and two common blooming seaweeds (Ulva rigida and Gracilaria vermiculophylla) in coastal lagoon sediments, on the structure of bacterial communities (using 16S rRNA amplicon sequencing) and corresponding putative functional potential (using PiCRUSt). At the Operational Taxonomic Unit (OTU) level, the addition of nutrients reduced bacterial community α-diversity and decreased the abundance of sulfate reducers (Desulfobacterales) compared to sulfur oxidizers/denitrifiers (Chromatiales and Campylobacterales), whereas this was not the case at the order level. Seaweed addition did not change bacterial α-diversity and the effect on community structure depended on the taxonomic level considered. The addition of Gracilaria increased the abundance of orders and OTUs involved in sulfate reduction and organic matter decomposition (Desulfobacterales, Bacteroidales, and Clostridiales, respectively), an effect which was also detected when only Ulva was added. Nutrients and the seaweeds combined only interacted for Ulva and nutrients, which increased known sulfide oxidizers and denitrifiers (order Campylobacterales). Seaweed enrichment affected putative functional profiles; a stronger increase of sulfur cycling KEGG pathways was assigned to nutrient-disturbed sediments, particularly with the seaweeds and especially Ulva. In contrast, nitrogen and sulfur cycle pathways showed a higher abundance of genes related to dissimilatory nitrate reduction to ammonium (DNRA) in Ulva+nutrients treatments. However, the other seaweed treatments increased the nitrogen fixation genes. Thiosulfate reduction, performed by sulfate-reducing bacteria, increased in seaweed treatments except when Ulva was combined with nutrients. In conclusion, the in situ addition of nutrients and the seaweeds to intertidal sediments affected the bacterial communities differently and independently. The predicted functional profile suggests a shift in relative abundances of putative pathways for nitrogen and sulfur cycles, in line with the taxonomic changes of the bacterial communities.
- Shifts in sulphur-cycling bacteria in the rhizobiome support the adaptation of Caulerpa prolifera to elevated sulphide levelsPublication . Barilo, Anastasiia; Engelen, Aschwin; Wilken, Susanne; Bouwmeester, Harro; Muyzer, GerardCaulerpa is a genus of green macroalgae that lives in tropical and subtropical coastal waters. It is an intriguing organism because, despite having plant-like structures, it is one giant cell – which, next to multiple nuclei, chloroplasts, and mitochondria, also contains endo- and epiphytic bacteria. The role of these bacteria is unknown, but they might impact the growth and development of the host, adaptation to environmental parameters, and, hence, the ecological success of these algae. We hypothesised that increased sulphide concentrations would trigger a significant shift in the microbial community composition associated with C. prolifera rhizoids, favouring sulphide-oxidizing bacteria. To test this hypothesis, we conducted a mesocosm experiment incubating C. prolifera in sediments with different sulphide concentrations and analysed the algal photosynthesis, growth, and microbiome composition. While photosynthesis was not affected, the Caulerpa weight-based growth rate decreased linearly with increasing sulphide concentration. To analyse the microbiome, we extracted DNA and RNA from the fronds, rhizoids, and the accompanying sediments and performed 16S amplicon sequencing. The microbiome of the fronds was unaffected in both the DNA and RNA samples. However, an increase in sulphide concentration coincided with a decrease in the relative abundance of sulphate-reducing bacteria associated with Caulerpa rhizoids, particularly from the family Desulfocapsaceae. In the RNA samples, potential sulphide oxidisers of the rhizoid-associated members of the Beggiatoaceae were detected. Our results suggest that the rhizobiome of Caulerpa plays a significant role in its adaptation to sulphide-rich environments, offering new insights into the complex interactions within marine holobionts.