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 Mechanisms
Invasive 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 wh...
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Frontiers Media S.A.
2021-08-01
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Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.653998/full |
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doaj-95b582e939f64027ade98e09a4b2d197 |
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Article |
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DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Tania Aires Tamara M. Stuij Tamara M. Stuij Gerard Muyzer Ester A. Serrão Aschwin H. Engelen Aschwin H. Engelen |
spellingShingle |
Tania Aires Tamara M. Stuij Tamara M. Stuij Gerard Muyzer Ester A. Serrão Aschwin H. Engelen Aschwin H. Engelen 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 Mechanisms Frontiers in Microbiology seagrasses invasions adaptation host–microbe interaction drivers of microbiome marine holobionts |
author_facet |
Tania Aires Tamara M. Stuij Tamara M. Stuij Gerard Muyzer Ester A. Serrão Aschwin H. Engelen Aschwin H. Engelen |
author_sort |
Tania Aires |
title |
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 Mechanisms |
title_short |
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 Mechanisms |
title_full |
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 Mechanisms |
title_fullStr |
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 Mechanisms |
title_full_unstemmed |
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 Mechanisms |
title_sort |
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 mechanisms |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Microbiology |
issn |
1664-302X |
publishDate |
2021-08-01 |
description |
Invasive 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. |
topic |
seagrasses invasions adaptation host–microbe interaction drivers of microbiome marine holobionts |
url |
https://www.frontiersin.org/articles/10.3389/fmicb.2021.653998/full |
work_keys_str_mv |
AT taniaaires characterizationandcomparisonofbacterialcommunitiesofaninvasiveandtwonativecaribbeanseagrassspeciesshedslightonthepossibleinfluenceofthemicrobiomeoninvasivemechanisms AT tamaramstuij characterizationandcomparisonofbacterialcommunitiesofaninvasiveandtwonativecaribbeanseagrassspeciesshedslightonthepossibleinfluenceofthemicrobiomeoninvasivemechanisms AT tamaramstuij characterizationandcomparisonofbacterialcommunitiesofaninvasiveandtwonativecaribbeanseagrassspeciesshedslightonthepossibleinfluenceofthemicrobiomeoninvasivemechanisms AT gerardmuyzer characterizationandcomparisonofbacterialcommunitiesofaninvasiveandtwonativecaribbeanseagrassspeciesshedslightonthepossibleinfluenceofthemicrobiomeoninvasivemechanisms AT esteraserrao characterizationandcomparisonofbacterialcommunitiesofaninvasiveandtwonativecaribbeanseagrassspeciesshedslightonthepossibleinfluenceofthemicrobiomeoninvasivemechanisms AT aschwinhengelen characterizationandcomparisonofbacterialcommunitiesofaninvasiveandtwonativecaribbeanseagrassspeciesshedslightonthepossibleinfluenceofthemicrobiomeoninvasivemechanisms AT aschwinhengelen characterizationandcomparisonofbacterialcommunitiesofaninvasiveandtwonativecaribbeanseagrassspeciesshedslightonthepossibleinfluenceofthemicrobiomeoninvasivemechanisms |
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doaj-95b582e939f64027ade98e09a4b2d1972021-08-09T14:17:25ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-08-011210.3389/fmicb.2021.653998653998Characterization 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 MechanismsTania Aires0Tamara M. Stuij1Tamara M. Stuij2Gerard Muyzer3Ester A. Serrão4Aschwin H. Engelen5Aschwin H. Engelen6Centro de Ciências do Mar (CCMAR), Centro de Investigação Marinha e Ambiental (CIMAR), Universidade do Algarve, Faro, PortugalCentro de Ciências do Mar (CCMAR), Centro de Investigação Marinha e Ambiental (CIMAR), Universidade do Algarve, Faro, PortugalCESAM - Centre for Environmental and Marine Studies, Department of Biology, University of Aveiro, Aveiro, PortugalMicrobial Systems Ecology, Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, NetherlandsCentro de Ciências do Mar (CCMAR), Centro de Investigação Marinha e Ambiental (CIMAR), Universidade do Algarve, Faro, PortugalCentro de Ciências do Mar (CCMAR), Centro de Investigação Marinha e Ambiental (CIMAR), Universidade do Algarve, Faro, PortugalCARMABI Foundation, Willemstad, CuraçaoInvasive 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.https://www.frontiersin.org/articles/10.3389/fmicb.2021.653998/fullseagrassesinvasionsadaptationhost–microbe interactiondrivers of microbiomemarine holobionts |