skip to main content

Attention:

The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 11:00 PM ET on Thursday, May 23 until 2:00 AM ET on Friday, May 24 due to maintenance. We apologize for the inconvenience.


Title: Environment and Co-occurring Native Mussel Species, but Not Host Genetics, Impact the Microbiome of a Freshwater Invasive Species (Corbicula fluminea)
The Asian clam Corbicula fluminea (Family: Cyneridae) has aggressively invaded freshwater habitats worldwide, resulting in dramatic ecological changes and declines of native bivalves such as freshwater mussels (Family: Unionidae), one of the most imperiled faunal groups. Despite increases in our knowledge of invasive C. fluminea biology, little is known of how intrinsic and extrinsic factors, including co-occurring native species, influence its microbiome. We investigated the gut bacterial microbiome across genetically differentiated populations of C. fluminea in the Tennessee and Mobile River Basins in the Southeastern United States and compared them to those of six co-occurring species of native freshwater mussels. The gut microbiome of C. fluminea was diverse, differed with environmental conditions and varied spatially among rivers, but was unrelated to host genetic variation. Microbial source tracking suggested that the gut microbiome of C. fluminea may be influenced by the presence of co-occurring native mussels. Inferred functions from 16S rRNA gene data using PICRUST2 predicted a high prevalence and diversity of degradation functions in the C. fluminea microbiome, especially the degradation of carbohydrates and aromatic compounds. Such modularity and functional diversity of the microbiome of C. fluminea may be an asset, allowing to acclimate to an extensive range of nutritional sources in invaded habitats, which could play a vital role in its invasive success.  more » « less
Award ID(s):
1831512 1831531
NSF-PAR ID:
10344513
Author(s) / Creator(s):
; ; ; ; ; ; ; ;
Date Published:
Journal Name:
Frontiers in Microbiology
Volume:
13
ISSN:
1664-302X
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Freshwater mussels perform essential ecosystem functions, yet we have no information on how their microbiomes fluctuate over time. In this study, we examined temporal variation in the microbiome of six mussel species (Lampsilis ornata, Obovaria unicolor, Elliptio arca, Fusconaia cerina, Cyclonaias asperata, and Tritogonia verrucosa) sampled from the same river in 2016 and 2019. We examined the taxonomic, phylogenetic, and inferred functional (from 16S rRNA sequences) facets of their microbiome diversity. Significant differences between the two years were identified in five of the six species sampled. However, not all species that exhibited a temporally variable microbiome were functionally distinct across years, indicating functional redundancy within the mussel gut microbiome. Inferred biosynthesis pathways showed temporal variation in pathways involved in degradation, while pathways involved in cellular metabolism were stable. There was no evidence for phylosymbiosis across any facet of microbiome biodiversity. These results indicate that temporal variation is an important factor in the assembly of the gut microbiomes of freshwater mussels and provides further support that the mussel gut microbiome is involved in host development and activity. 
    more » « less
  2. Abstract

    Mammalian gut microbiomes differ within and among hosts. Hosts that occupy a broad range of environments may exhibit greater spatiotemporal variation in their microbiome than those constrained as specialists to narrower subsets of resources or habitats. This can occur if widespread host encounter a variety of ecological conditions that act to diversify their gut microbiomes and/or if generalized host species tend to form large populations that promote sharing and maintenance of diverse microbes. We studied spatiotemporal variation in the gut microbiomes of three co‐occurring rodent species across an environmental gradient in a Kenyan savanna. We hypothesized: (1) the taxonomic, phylogenetic, and functional compositions of gut microbiomes as predicted using the Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) differ significantly among host species; (2) microbiome richness increases with population size for all host species; and (3) host species exhibit different levels of seasonal change in their gut microbiomes, reflecting different sensitivities to the environment. We evaluated changes in gut microbiome composition according to host species identity, site, and host population size using three years of capture–mark–recapture data and 351 microbiome samples. Host species differed significantly in microbiome composition, though the two species with more specialized diets and higher demographic sensitivities showed only slightly greater microbiome variability than those of a widespread dietary generalist. Total microbiome richness increased significantly with host population size for all species, but only one of the more specialized species also exhibited greater individual‐level microbiome richness in large populations. Across co‐occurring rodent species with diverse diets and life histories, large host population sizes were associated both with greater population‐level microbiome richness (sampling effects) and turnover in the relative abundance of bacterial taxa (environmental effects), but there was no consistent pattern for individual‐level richness (individual specialization). Together, our results show that maintenance of large host populations contributes to the maintenance of gut microbiome diversity in wild mammals.

     
    more » « less
  3. Abstract Background

    Understanding the factors that influence microbes’ environmental distributions is important for determining drivers of microbial community composition. These include environmental variables like temperature and pH, and higher-dimensional variables like geographic distance and host species phylogeny. In microbial ecology, “specificity” is often described in the context of symbiotic or host parasitic interactions, but specificity can be more broadly used to describe the extent to which a species occupies a narrower range of an environmental variable than expected by chance. Using a standardization we describe here, Rao’s (Theor Popul Biol, 1982. https://doi.org/10.1016/0040-5809(82)90004-1, Sankhya A, 2010. https://doi.org/10.1007/s13171-010-0016-3 ) Quadratic Entropy can be conveniently applied to calculate specificity of a feature, such as a species, to many different environmental variables.

    Results

    We present our R packagespecificityfor performing the above analyses, and apply it to four real-life microbial data sets to demonstrate its application. We found that many fungi within the leaves of native Hawaiian plants had strong specificity to rainfall and elevation, even though these variables showed minimal importance in a previous analysis of fungal beta-diversity. In Antarctic cryoconite holes, our tool revealed that many bacteria have specificity to co-occurring algal community composition. Similarly, in the human gut microbiome, many bacteria showed specificity to the composition of bile acids. Finally, our analysis of the Earth Microbiome Project data set showed that most bacteria show strong ontological specificity to sample type. Our software performed as expected on synthetic data as well.

    Conclusions

    specificityis well-suited to analysis of microbiome data, both in synthetic test cases, and across multiple environment types and experimental designs. The analysis and software we present here can reveal patterns in microbial taxa that may not be evident from a community-level perspective. These insights can also be visualized and interactively shared among researchers usingspecificity’s companion package,specificity.shiny.

     
    more » « less
  4. Abstract

    Freshwater mussels are important for nutrient cycling and ecosystem health as they filter feed on their surrounding water. This filter feeding makes these bivalves especially sensitive to conditions in their environment. Gut microbial communities (microbiomes) have been recognised as important to both host organism and ecosystem health; however, how freshwater mussel microbiomes are organised and influenced is unclear.

    In this study, the gut bacterial microbiome of Threeridge mussel,Amblema plicata, was compared across two river basins, five rivers, and nine local sites in the south‐eastern U.S.A. Mussel gut tissue was dissected, DNA extracted, and the microbiome characterised by high throughput sequencing of the V4 region of the 16S ribosomal RNA gene.

    Planctomycetes, Firmicutes, and Cyanobacteria were the most common bacterial phyla within the guts of all sampledA.plicata. However, the relative abundances of these major bacterial phyla differed between mussels sampled from different rivers and river basins, as did the relative abundance of specific bacterial operational taxonomic units (OTUs). Despite these differences, a core microbiome was identified across all mussels, with eight OTUs being consistent members of theA.plicatamicrobiome at all sites, the most abundant OTU identifying as a member of the family Planctomycetaceae. Geographic distance between sites was not correlated with similarity in the structure of the gut microbiome, which was more related to site physicochemistry.

    Overall, these results suggest that while physicochemical conditions affect the composition of transient bacteria in the Threeridge mussel gut microbiome, the core microbiome is largely unaffected, and a portion of theA.plicatamicrobiome is retained regardless of the river system.

    How long transient bacteria remain in the gut, and to what extent these transient microbes aid in host function is still unknown. Core microbiota have been found to aid in multiple functions within animal hosts, and within freshwater mussels this core microbiome may aid in nutrient processing and cycling. Therefore, it is important to look at both transient and core microbes when studying the structure of freshwater invertebrate microbiomes.

     
    more » « less
  5. Abstract

    This study aimed to identify the importance of ecological factors to distribution patterns of the invasive Clam (Corbicula fluminea) relative to native mussels (family: Unionidae) across seven rivers within the Mobile and Tennessee basins, Southeast United States. We quantitatively surveyed dense, diverse native mussel aggregations across 20 river reaches and estimated mussel density, biomass, and species richness along with density of invasiveC.fluminea(hereafterCorbicula). We measured substrate particle size, velocity, and depth in quadrats where animals were collected. Additionally, we characterized reach scale environmental parameters including seston quantity and quality (% Carbon, % Nitrogen, % Phosphorous), water chemistry (ammonium [], soluble reactive phosphorous [SRP]), and watershed area and land cover. Using model selection, logistic regression, and multivariate analysis, we characterized habitat features and their association to invasiveCorbiculawithin mussel beds. We found thatCorbiculawere more likely to occur and more abundant in quadrats with greater mussel biomass, larger substrate size, faster water velocity, and shallower water depth. At the reach scale,Corbiculadensities increased where particle sizes were larger. Mussel richness, density, and biomass increased with watershed area. Water column increased at reaches with more urban land cover. No land cover variables influencedCorbiculapopulations or mussel communities. The strong overlapping distribution ofCorbiculaand mussels support the hypothesis thatCorbiculaare not necessarily limited by habitat factors and may be passengers of change in rivers where mussels have declined due to habitat degradation. WhetherCorbiculais facilitated by mussels or negatively interacts with mussels in these systems remains to be seen. Focused experiments that manipulate patch scale variables would improve our understanding of the role of species interactions (e.g., competition, predation, facilitation) or physical habitat factors in influencing spatial overlap betweenCorbiculaand native mussels.

     
    more » « less