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 Caulerpa racemosa 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.

Highlights

  • Anthropogenic disturbances inducing habitat change, modification of biotic interactions and deliberated or accidental translocation of specimens outside their species distribution range are propelling a global increase in biological invasions [1,2]

  • The total of 173512 sequences used in downstream analysis after quality control (Table S1) revealed 18325 bacterial Operational Taxonomic Units (OTUs) that segregate into three distinct clusters (Figure 1A)

  • Results reported here show an extreme diversity of bacterial OTUs associated to C. racemosa (Table S2) both in its native and in its invasive range, reaching or exceeding the already high level of diversity reported for exceptional holobionts such as coral or sponges systems [24]

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Summary

Introduction

Anthropogenic disturbances inducing habitat change, modification of biotic interactions and deliberated or accidental translocation of specimens outside their species distribution range are propelling a global increase in biological invasions [1,2]. In turn, are additional drivers of biodiversity decline [3]. The capacity of introduced species to expand and become invasive is dependent on their capacity to adapt to new environmental conditions. Assessments of the potential of introduced species for invasive behavior have focused on the role of morphological and physiological traits as drivers of their potential to outcompete native species [4,5]. The competitive potential of invasive species may not be entirely determined by their intrinsic capacities, but may be at least partly shaped by associated microbes[6]. Our understanding of the mechanisms underlying the establishment and spread of introduced species may require a serious appraisal of the potential co-introduction and influence of bacterial communities on the success of non-indigenous species

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