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Invasion is a community affair: Clandestine followers in the bacterial community associated to green algae, Caulerpa racemosa, track the invasion source.

Aires T, Serrão EA, Kendrick G, Duarte CM, Arnaud-Haond S - PLoS ONE (2013)

Bottom Line: Indirect inferences on the taxonomic identity and associated metabolism of bacterial lineages showed a striking consistency with sediment upheaval conditions associated to the expansion of their invasive host and to the decline of native species.These results demonstrate that bacterial communities can be an effective tracer of the origin of invasion and support their potential role in their eukaryotic host's adaptation to new environments.They put forward the critical need to consider the 'meta-organism' encompassing both the host and associated micro-organisms, to unravel the origins, causes and mechanisms underlying biological invasions.

View Article: PubMed Central - PubMed

Affiliation: Center for Marine Sciences, University of Algarve, Faro, Portugal.

ABSTRACT
Biological invasions rank amongst the most deleterious components of global change inducing alterations from genes to ecosystems. The genetic characteristics of introduced pools of individuals greatly influence the capacity of introduced species to establish and expand. The recently demonstrated heritability of microbial communities associated to individual genotypes of primary producers makes them a potentially essential element of the evolution and adaptability of their hosts. Here, we characterized the bacterial communities associated to native and non-native populations of the marine green macroalga Caulerparacemosa through pyrosequencing, and explored their potential role on the strikingly invasive trajectory of their host in the Mediterranean. The similarity of endophytic bacterial communities from the native Australian range and several Mediterranean locations confirmed the origin of invasion and revealed distinct communities associated to a second Mediterranean variety of C. racemosa long reported in the Mediterranean. Comparative analysis of these two groups demonstrated the stability of the composition of bacterial communities through the successive steps of introduction and invasion and suggested the vertical transmission of some major bacterial OTUs. Indirect inferences on the taxonomic identity and associated metabolism of bacterial lineages showed a striking consistency with sediment upheaval conditions associated to the expansion of their invasive host and to the decline of native species. These results demonstrate that bacterial communities can be an effective tracer of the origin of invasion and support their potential role in their eukaryotic host's adaptation to new environments. They put forward the critical need to consider the 'meta-organism' encompassing both the host and associated micro-organisms, to unravel the origins, causes and mechanisms underlying biological invasions.

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PCA representing weighted Unifrac analysis of C. racemosa samples from Mediterranean Sea and Australia (invaded and native range), A-All samples including controls; B-Disinfected samples only.Sample Codes: Al- Albany (Australia), CB- Cottesloe Beach (Australia), Lg- Liguria (Greece), AP- Agios Pavlo (Greece), Ml- Malta, M-Marseille, I- Illetas (Mallorca, Spain), EsC- Es Cargol (Mallorca, Spain), RI1- Rottnest Island 1 (Australia), RI2- Rottnest Island 2 (Australia), TN- Tunisia, VF- Villefranche (France).
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pone-0068429-g001: PCA representing weighted Unifrac analysis of C. racemosa samples from Mediterranean Sea and Australia (invaded and native range), A-All samples including controls; B-Disinfected samples only.Sample Codes: Al- Albany (Australia), CB- Cottesloe Beach (Australia), Lg- Liguria (Greece), AP- Agios Pavlo (Greece), Ml- Malta, M-Marseille, I- Illetas (Mallorca, Spain), EsC- Es Cargol (Mallorca, Spain), RI1- Rottnest Island 1 (Australia), RI2- Rottnest Island 2 (Australia), TN- Tunisia, VF- Villefranche (France).

Mentions: The total of 173512 sequences used in downstream analysis after quality control (Table S1) revealed 18325 bacterial Operational Taxonomic Units (OTUs) (represented by unique 16S genotypes) that segregate into three distinct clusters (Figure 1A). These results allowed us to distinguish total communities including epiphytic bacteria (i.e., samples from non-treated algae) and sediment samples versus the other two groups composed of endophytic communities (i.e., bleached algal samples free of epiphytes and of chloroplasts). In order to understand how endophytic bacteria would shape the different populations, the same analyses were applied just on the disinfected samples allowing us to look deeper into the endophytic community structure. Results show that populations were separated into 2 clusters. Cluster A gathered samples just from Mediterranean sites including Tunis, Villefranche and Greece, and Cluster B joined samples from Malta, Marseille and Mallorca with samples from Australian native range (WA) (Figure 1B). This discrimination of three groups by the Principal Component Analysis (PCA) was strongly supported (p<0.01) by the analysis of community similarity (ANOSIM) using Bray-Curtis distances (Table S3). The clustering of non-disinfected and sediment samples apart from disinfected samples suggests the distinct composition of endophytic compared to putative epiphytic communities that clearly appear to be more similar to the environmental ones (from sediment) (Figure 1A). The Venn diagram drawn from an OTU table pooling samples from the different treatments, shows that non-disinfected samples and sediment share the highest percentage of OTUs -12.87% (Figure 2). In the case of the percentage of OTUs shared between disinfected and non-disinfected samples (8.78%) (Figure 2) it is mostly driven by OTUs that appeared as shared due to a single sequence in the first pool vs thousands of the same OTU in the other, reflecting the very scarce persistence in the surface disinfected samples of some bacteria that are mostly epiphytic.


Invasion is a community affair: Clandestine followers in the bacterial community associated to green algae, Caulerpa racemosa, track the invasion source.

Aires T, Serrão EA, Kendrick G, Duarte CM, Arnaud-Haond S - PLoS ONE (2013)

PCA representing weighted Unifrac analysis of C. racemosa samples from Mediterranean Sea and Australia (invaded and native range), A-All samples including controls; B-Disinfected samples only.Sample Codes: Al- Albany (Australia), CB- Cottesloe Beach (Australia), Lg- Liguria (Greece), AP- Agios Pavlo (Greece), Ml- Malta, M-Marseille, I- Illetas (Mallorca, Spain), EsC- Es Cargol (Mallorca, Spain), RI1- Rottnest Island 1 (Australia), RI2- Rottnest Island 2 (Australia), TN- Tunisia, VF- Villefranche (France).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3713043&req=5

pone-0068429-g001: PCA representing weighted Unifrac analysis of C. racemosa samples from Mediterranean Sea and Australia (invaded and native range), A-All samples including controls; B-Disinfected samples only.Sample Codes: Al- Albany (Australia), CB- Cottesloe Beach (Australia), Lg- Liguria (Greece), AP- Agios Pavlo (Greece), Ml- Malta, M-Marseille, I- Illetas (Mallorca, Spain), EsC- Es Cargol (Mallorca, Spain), RI1- Rottnest Island 1 (Australia), RI2- Rottnest Island 2 (Australia), TN- Tunisia, VF- Villefranche (France).
Mentions: The total of 173512 sequences used in downstream analysis after quality control (Table S1) revealed 18325 bacterial Operational Taxonomic Units (OTUs) (represented by unique 16S genotypes) that segregate into three distinct clusters (Figure 1A). These results allowed us to distinguish total communities including epiphytic bacteria (i.e., samples from non-treated algae) and sediment samples versus the other two groups composed of endophytic communities (i.e., bleached algal samples free of epiphytes and of chloroplasts). In order to understand how endophytic bacteria would shape the different populations, the same analyses were applied just on the disinfected samples allowing us to look deeper into the endophytic community structure. Results show that populations were separated into 2 clusters. Cluster A gathered samples just from Mediterranean sites including Tunis, Villefranche and Greece, and Cluster B joined samples from Malta, Marseille and Mallorca with samples from Australian native range (WA) (Figure 1B). This discrimination of three groups by the Principal Component Analysis (PCA) was strongly supported (p<0.01) by the analysis of community similarity (ANOSIM) using Bray-Curtis distances (Table S3). The clustering of non-disinfected and sediment samples apart from disinfected samples suggests the distinct composition of endophytic compared to putative epiphytic communities that clearly appear to be more similar to the environmental ones (from sediment) (Figure 1A). The Venn diagram drawn from an OTU table pooling samples from the different treatments, shows that non-disinfected samples and sediment share the highest percentage of OTUs -12.87% (Figure 2). In the case of the percentage of OTUs shared between disinfected and non-disinfected samples (8.78%) (Figure 2) it is mostly driven by OTUs that appeared as shared due to a single sequence in the first pool vs thousands of the same OTU in the other, reflecting the very scarce persistence in the surface disinfected samples of some bacteria that are mostly epiphytic.

Bottom Line: Indirect inferences on the taxonomic identity and associated metabolism of bacterial lineages showed a striking consistency with sediment upheaval conditions associated to the expansion of their invasive host and to the decline of native species.These results demonstrate that bacterial communities can be an effective tracer of the origin of invasion and support their potential role in their eukaryotic host's adaptation to new environments.They put forward the critical need to consider the 'meta-organism' encompassing both the host and associated micro-organisms, to unravel the origins, causes and mechanisms underlying biological invasions.

View Article: PubMed Central - PubMed

Affiliation: Center for Marine Sciences, University of Algarve, Faro, Portugal.

ABSTRACT
Biological invasions rank amongst the most deleterious components of global change inducing alterations from genes to ecosystems. The genetic characteristics of introduced pools of individuals greatly influence the capacity of introduced species to establish and expand. The recently demonstrated heritability of microbial communities associated to individual genotypes of primary producers makes them a potentially essential element of the evolution and adaptability of their hosts. Here, we characterized the bacterial communities associated to native and non-native populations of the marine green macroalga Caulerparacemosa through pyrosequencing, and explored their potential role on the strikingly invasive trajectory of their host in the Mediterranean. The similarity of endophytic bacterial communities from the native Australian range and several Mediterranean locations confirmed the origin of invasion and revealed distinct communities associated to a second Mediterranean variety of C. racemosa long reported in the Mediterranean. Comparative analysis of these two groups demonstrated the stability of the composition of bacterial communities through the successive steps of introduction and invasion and suggested the vertical transmission of some major bacterial OTUs. Indirect inferences on the taxonomic identity and associated metabolism of bacterial lineages showed a striking consistency with sediment upheaval conditions associated to the expansion of their invasive host and to the decline of native species. These results demonstrate that bacterial communities can be an effective tracer of the origin of invasion and support their potential role in their eukaryotic host's adaptation to new environments. They put forward the critical need to consider the 'meta-organism' encompassing both the host and associated micro-organisms, to unravel the origins, causes and mechanisms underlying biological invasions.

Show MeSH
Related in: MedlinePlus