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Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra.

ABSTRACT: Epithelia in animals are colonized by complex communities of microbes. Although a topic of long-standing interest, understanding the evolution of the microbial communities and their role in triggering innate immune responses has resisted analysis. Cnidaria are among the simplest animals at the tissue grade of organization. To obtain a better understanding of the microbiota associated with phylogenetically ancient epithelia, we have identified the epibiotic and endosymbiotic bacteria of two species of the cnidarian Hydra on the basis of rRNA comparisons. We analyzed individuals of Hydra oligactis and Hydra vulgaris from both laboratory cultures and the wild. We discovered that individuals from both species differ greatly in their bacterial microbiota. Although H. vulgaris polyps have a quite diverse microbiota, H. oligactis appears to be associated with only a limited number of microbes; some of them were found, unexpectedly, to be endosymbionts. Surprisingly, the microfauna showed similar characteristics in individuals of cultures maintained in the laboratory for >30 years and polyps directly isolated from the wild. The significant differences in the microbial communities between the two species and the maintenance of specific microbial communities over long periods of time strongly indicate distinct selective pressures imposed on and within the epithelium. Our analysis suggests that the Hydra epithelium actively selects and shapes its microbial community.

SUBMITTER: Fraune S

PROVIDER: S-EPMC1934924 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Next-generation sequencing has greatly contributed to an improved ecological understanding of the human gut microbiota. Nevertheless, questions remain regarding the characteristics of this ecosystem and the ecological processes that shape it, and controversy has arisen regarding the stability of the bacterial populations and the existence of a temporal core. In this study, we have characterized the fecal microbial communities of three human individuals over a one-year period by 454 pyrosequencing of 16S rRNA tags in order to investigate the temporal characteristics of the bacterial communities. The findings revealed a temporal core of 33 to 40 species-level Operational Taxonomic Units (OTUs) within subjects. Although these OTUs accounted only for around 12% of the total OTUs detected, they added up to >75% of the total sequences obtained for each individual. In order to determine the capacity of the sequencing and bioinformatic approaches applied during this study to accurately determine the proportion of a core microbiota, we analyzed the fecal microbiota of nine mice with a defined three-member community. This experiment revealed that the sequencing approach inflated the amount of rare OTUs, which introduced a significant degree of artificial variation across samples, and hence reduced the apparent fraction of shared OTUs. However, when assessing the data quantitatively by focusing on dominant lineages, the sequencing approaches deliver an accurate representation of the community. In conclusion, this study revealed that the human fecal microbiota is dominated by around 40 species that maintain persistent populations over the duration of one year. The findings allow conclusions about the ecological factors that shape the community and support the concept of a homeostatic ecosystem controlled largely by deterministic processes. Our analysis of a three-member community revealed that methodological artifacts of OTU-based approaches complicate core calculations, and these limitations have to be considered in the interpretation of microbiome studies.

Project description:BACKGROUND: Animal mitochondrial (mt) genomes are characteristically circular molecules of approximately 16-20 kb. Medusozoa (Cnidaria excluding Anthozoa) are exceptional in that their mt genomes are linear and sometimes subdivided into two to presumably four different molecules. In the genus Hydra, the mt genome comprises one or two mt chromosomes. Here, we present the whole mt genome sequence from the hydrozoan Hydra magnipapillata, comprising the first sequence of a fragmented metazoan mt genome encoded on two linear mt chromosomes (mt1 and mt2). RESULTS: The H. magnipapillata mt chromosomes contain the typical metazoan set of 13 genes for respiratory proteins, the two rRNA genes and two tRNA genes. All genes are unidirectionally oriented on mt1 and mt2, and several genes overlap. The gene arrangement suggests that the two mt chromosomes originated from one linear molecule that separated between nd5 and rns. Strong correlations between the AT content of rRNA genes (rns and rnl) and the AT content of protein-coding genes among 24 cnidarian genomes imply that base composition is mainly determined by mt genome-wide constraints. We show that identical inverted terminal repeats (ITR) occur on both chromosomes; these ITR contain a partial copy or part of the 3' end of cox1 (54 bp). Additionally, both mt chromosomes possess identical oriented sequences (IOS) at the 5' and 3' ends (5' and 3' IOS) adjacent to the ITR. The 5' IOS contains trnM and non-coding sequences (119 bp), whereas the 3' IOS comprises a larger part (mt2) with a larger partial copy of cox1 (243 bp). CONCLUSION: ITR are also documented in the two other available medusozoan mt genomes (Aurelia aurita and Hydra oligactis). In H. magnipapillata, the arrangement of ITR and 5' IOS and 3' IOS suggest that these regions are crucial for mt DNA replication and/or transcription initiation. An analogous organization occurs in a highly fragmented ichthyosporean mt genome. With our data, we can reject a model of mt replication that has previously been proposed for Hydra. This raises new questions regarding replication mechanisms probably employed by all medusozoans, and also has general implications for the expected organization of fragmented linear mt chromosomes of other taxa.

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Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra.

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