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Environmental Influence and Species Specificity of Microbiome Structure and Composition Microbial Ecology (2018) 76:467–481 https://doi.org/10.1007/s00248-017-1134-4 INVERTEBRATE MICROBIOLOGY The Microbial Community of Tardigrades: Environmental Influence and Species Specificity of Microbiome Structure and Composition Matteo Vecchi1 & Irene L.G. Newton2 & Michele Cesari1 & Lorena Rebecchi1 & Roberto Guidetti1 Received: 4 May 2017 /Accepted: 19 December 2017 /Published online: 15 January 2018 # Springer Science+Business Media, LLC, part of Springer Nature 2018 Abstract Symbiotic associations of metazoans with bacteria strongly influence animal biology since bacteria are ubiquitous and virtually no animal is completely free from them. Tardigrades are micrometazoans famous for their ability to undergo ametabolic states (cryptobiosis) but very little information is available on potential microbial associations. We characterized the microbiomes of six limnoterrestrial tardigrade species belonging to several phylogenetic lines in tandem with the microbiomes of their respective substrates. The experimental design enabled us to determine the effects of both the environment and the host genetic background on the tardigrade microbiome; we were able to define the microbial community of the same species sampled from different environments, and the communities of different species from the same environment. Our 16S rRNA gene amplicon approach indicated that the tardigrade microbiome is species-specific and well differentiated from the environment. Tardigrade species showed a much lower microbial diversity compared to their substrates, with only one significant exception. Forty-nine common OTUs (operational taxonomic units) were classified into six bacterial phyla, while four common OTUs were unclassified and probably represent novel bacterial taxa. Specifically, the tardigrade microbiome appears dominated by Proteobacteria and Bacteroidetes. Some OTUs were shared between different species from geographically distant samples, suggesting the associated bacteria may be widespread. Putative endosymbionts of tardigrades from the order Rickettsiales were identified. Our results indicated that like all other animals, tardigrades have their own microbiota that is different among species, and its assembly is determined by host genotype and environmental influences. Keywords Endosymbiont . Microbiome . Rickettsiales . Symbiosis . Tardigrada Introduction Tardigrada (water bears; Fig. 1) is a phylum of poorly studied known phylum has recently increased as a consequence of ecdysozoan animals, ubiquitous in their distribution (present some of their biological properties (see [3]). Thanks to their worldwide in marine and continental environments) and fa- abilities to withstand physical and chemical extremes, tardi- mous for their ability to survive strong environmental grades have become model organisms for space research stressors such as desiccation (anhydrobiosis) and freezing [4–9], and for the study of the molecular mechanisms behind (cryobiosis) (for a review see [1, 2]). Interest in this scarcely the anhydrobiotic process [10–13]. Moreover, due to their position in the tree of life, tardigrades are recognized as a key taxon in the study of animal phylogeny and evolutionary Electronic supplementary material The online version of this article – (https://doi.org/10.1007/s00248-017-1134-4) contains supplementary developmental biology [14 18]. Lastly, a recent controversy material, which is available to authorized users. has arisen about the tardigrade genome, specifically regarding the number of genes derived from horizontal gene transfer * Matteo Vecchi (HGT) between bacteria and the model tardigrade Hypsibius [email protected] dujardini (Doyère, 1840) [19–24]. There are other important reasons to be interested in the 1 Department of Life Sciences, University of Modena and Reggio microbiota of the tardigrades. Bacterial associations with Emilia, Via Campi 213/D, 41125 Modena, Italy metazoans are currently recognized as a factor influencing 2 Department of Biology, Indiana University, Jordan Hall 221, 1001 E. many different aspects of animal biology such as metabolism 3rd St., Bloomington, IN 47405, USA [25], immunity [26], behavior [27], and perhaps speciation 468 Vecchi M. et al. influence their microbial community, perhaps constraining bacterial species that could develop a stable association with tardigrades, similarly to what was observed for rotifers [40]. Here, we characterized the tardigrade microbiota, paying particular attention to the following research questions: (i) Is the microbial community of tardigrades distinct from that of their habitat? (ii) Do tardigrades have a species-specific mi- crobial community? (iii) Do tardigrades have putative endo- symbionts? (iv) Is there a host-influenced phylogenetic signal in the microbial community composition of tardigrades? and (v) Does laboratory rearing influence the microbiome compo- sition of tardigrades? Materials and Methods Experimental Design and Analyzed Tardigrade Species Fig. 1 Scanning electron microscopy microphotograph of the For this study, six limnoterrestrial tardigrade species were cho- eutardigrade Macrobiotus macrocalix on moss leaflets sen. Along with the tardigrade microbiomes, we also character- ized the microbiome of the corresponding substrates colonized [28]. Indeed, many animals seem to harbor their own specific by tardigrades. To answer our research questions, we character- communities of bacteria and these have been characterized for ized the microbiome associated with the same tardigrade spe- a wide range of animal taxa, including sponges, cnidarians, cies (always along with the microbiome of its substrate) extract- insects, copepods, roundworms, and various vertebrate spe- ed from different samples, and the microbiomes associated with cies [29–34]. different tardigrade species extracted from the same sample. However, little is known about microbial communities in The seven analyzed samples (S1–S7) were grouped according- the so-called minor phyla, including tardigrades. Microbial ly to the substrates and/or tardigrade species of interest in four communities associated with tardigrades are scarcely or spo- experiments (Exp. 1: S1–S3, Exp. 2: S4–S5, Exp. 3: S6, Exp. 4: radically documented, and prior informations are found main- S7) for a better representation of bacterial abundance and data ly as marginal notes in ecological or taxonomic papers (for a analysis. Sampling details are reported in Table 1. review see [35]). One of the few experimental studies on the The tardigrade species considered for this study belong to bacteria associated with tardigrades [36] suggested a non- different evolutionary lineages: Echiniscus trisetosus Cuénot, random association between tardigrades and bacteria. In that 1932 (Heterotardigrada, Echiniscoidea, Echiniscidae); work, phytopathogenic bacteria (Xanthomonas sp. and Acutuncus antarcticus (Richters, 1904) (Eutardigrada, Serratia marcescens Bizio, 1823) differed in their ability to Hypsibioidea, Hypsibiidae); Ramazzottius oberhaeuseri persist in, or on, the tardigrade body. Generally, microbial (Doyère, 1840) (Eutardigrada, Hypsibioidea, symbionts can be both transmitted vertically from parents to Ramazzottiidae); Richtersius coronifer (Richters, 1903) offspring and acquired horizontally from the environment or (Eutardigrada, Macrobiotoidea, Richtersiidae); Macrobiotus from other individuals [37]. Therefore, microbial communi- macrocalix Bertolani & Rebecchi, 1993; and ties associated with tardigrades could comprise host-specific Paramacrobiotus areolatus (Murray, 1907) (Eutardigrada, bacteria, such as endosymbionts (as are often observed in Macrobiotoidea, Macrobiotidae). The sampled population of many arthropods; see [38]), and/or bacteria belonging to the E. trisetosus contained a mixture of different morphotypes Bcore microbiome^ (as observed in nematodes [39]). But the (E. trisetosus, E. medianthus, E. canadensis) belonging to bacterial communities of tardigrades would likely also contain the Echiniscus blumi-canadensis series (see [41]). The se- environmental and food-associated microbes. These hypothe- quencing of a fragment of the cox1 gene (DNA was extracted ses are not mutually exclusive, as the tardigrade microbiome from the animals with a modified HotSHOT protocol, see could consist of a mixture of lineages, including host-specific Supplementary Methods in Supporting Information and [42], microbes and environmentally derived ones, in different pro- and primers were taken from [43]) revealed that individuals of portions, and the number of which could vary for each tardi- the studied population of Echiniscus trisetosus (from S7) be- grade species. In addition, one might suppose that the longing to the three different morphotypes (canadensis, anhydrobiotic and cryobiotic capabilities of tardigrades could medianthus, trisetosus), all belong to the same species (for The Microbial Community of Tardigrades: Environmental Influence and Species Specificity of Microbiome... 469 Table 1 Experimental design and materials used in the study Experiments Sample Sample detailsa Tardigrade Number of Replicates code species/ replicates group codes substratesb Exp. 1 S1 Freshwater sediment frozen after collection Acutuncus 6S1_Acu1-6 Same tardigrade species Edmonson Point, Victoria Land, Antarctica antarcticus in different samples Lat. S 74.330733; Lon. E 165.135883 Substrate 5 S1_Sub 1-5 35 m a.s.l. (Lab. code C3647) S2 Dry freshwater sediment frozen after collection Acutuncus 6S2_Acu1-6 Terranova Bay, Victoria
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