skip to main content

Title: Assembly of wood-inhabiting archaeal, bacterial and fungal communities along a salinity gradient: common taxa are broadly distributed but locally abundant in preferred habitats

Wood decomposition in water is a key ecosystem process driven by diverse microbial taxa that likely differ in their affinities for freshwater, estuarine and marine habitats. How these decomposer communities assemble in situ or potentially colonize from other habitats remains poorly understood. At three watersheds on Coiba Island, Panama, we placed replicate sections of branch wood of a single tree species on land, and in freshwater, estuarine and marine habitats that constitute a downstream salinity gradient. We sequenced archaea, bacteria and fungi from wood samples collected after 3, 9 and 15 months to examine microbial community composition, and to examine habitat specificity and abundance patterns. We found that these microbial communities were broadly structured by similar factors, with a strong effect of salinity, but little effect of watershed identity on compositional variation. Moreover, common aquatic taxa were also present in wood incubated on land. Our results suggest that either taxa dispersed to both terrestrial and aquatic habitats, or microbes with broad habitat ranges were initially present in the wood as endophytes. Nonetheless, these habitat generalists varied greatly in abundance across habitats suggesting an important role for habitat filtering in maintaining distinct aquatic communities in freshwater, estuarine and marine habitats.

more » « less
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
FEMS Microbiology Ecology
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Background

    Annually reoccurring microbial populations with strong spatial and temporal variations have been identified in estuarine environments, especially in those with long residence time such as the Chesapeake Bay (CB). However, it is unclear how microbial taxa cooccurr and how the inter-taxa networks respond to the strong environmental gradients in the estuaries.


    Here, we constructed co-occurrence networks on prokaryotic microbial communities in the CB, which included seasonal samples from seven spatial stations along the salinity gradients for three consecutive years. Our results showed that spatiotemporal variations of planktonic microbiomes promoted differentiations of the characteristics and stability of prokaryotic microbial networks in the CB estuary. Prokaryotic microbial networks exhibited a clear seasonal pattern where microbes were more closely connected during warm season compared to the associations during cold season. In addition, microbial networks were more stable in the lower Bay (ocean side) than those in the upper Bay (freshwater side). Multivariate regression tree (MRT) analysis and piecewise structural equation modeling (SEM) indicated that temperature, salinity and total suspended substances along with nutrient availability, particulate carbon and Chla, affected the distribution and co-occurrence of microbial groups, such as Actinobacteria, Bacteroidetes, Cyanobacteria, Planctomycetes, Proteobacteria, and Verrucomicrobia. Interestingly, compared to the abundant groups (such as SAR11, Saprospiraceae and Actinomarinaceae), the rare taxa including OM60 (NOR5) clade (Gammaproteobacteria), Micrococcales (Actinobacteria), and NS11-12 marine group (Bacteroidetes) contributed greatly to the stability of microbial co-occurrence in the Bay. Modularity and cluster structures of microbial networks varied spatiotemporally, which provided valuable insights into the ‘small world’ (a group of more interconnected species), network stability, and habitat partitioning/preferences.


    Our results shed light on how estuarine gradients alter the spatiotemporal variations of prokaryotic microbial networks in the estuarine ecosystem, as well as their adaptability to environmental disturbances and co-occurrence network complexity and stability.

    more » « less
  2. Abstract

    Whole microbial communities regularly merge with one another, often in tandem with their environments, in a process called community coalescence. Such events impose substantial changes: abiotic perturbation from environmental blending and biotic perturbation of community merging. We used an aquatic mixing experiment to unravel the effects of these perturbations on the whole microbiome response and on the success of individual taxa when distinct freshwater and marine communities coalesce. We found that an equal mix of freshwater and marine habitats and blended microbiomes resulted in strong convergence of the community structure toward that of the marine microbiome. The enzymatic potential of these blended microbiomes in mixed media also converged toward that of the marine, with strong correlations between the multivariate response patterns of the enzymes and of community structure. Exposing each endmember inocula to an axenic equal mix of their freshwater and marine source waters led to a 96% loss of taxa from our freshwater microbiomes and a 66% loss from our marine microbiomes. When both inocula were added together to this mixed environment, interactions amongst the communities led to a further loss of 29% and 49% of freshwater and marine taxa, respectively. Under both the axenic and competitive scenarios, the diversity lost was somewhat counterbalanced by increased abundance of microbial taxa that were too rare to detect in the initial inocula. Our study emphasizes the importance of the rare biosphere as a critical component of microbial community responses to community coalescence.

    more » « less
  3. Abstract

    Despite the obstacles facing marine colonists, most lineages of aquatic organisms have colonized and diversified in freshwaters repeatedly. These transitions can trigger rapid morphological or physiological change and, on longer timescales, lead to increased rates of speciation and extinction. Diatoms are a lineage of ancestrally marine microalgae that have diversified throughout freshwater habitats worldwide. We generated a phylogenomic data set of genomes and transcriptomes for 59 diatom taxa to resolve freshwater transitions in one lineage, the Thalassiosirales. Although most parts of the species tree were consistently resolved with strong support, we had difficulties resolving a Paleocene radiation, which affected the placement of one freshwater lineage. This and other parts of the tree were characterized by high levels of gene tree discordance caused by incomplete lineage sorting and low phylogenetic signal. Despite differences in species trees inferred from concatenation versus summary methods and codons versus amino acids, traditional methods of ancestral state reconstruction supported six transitions into freshwaters, two of which led to subsequent species diversification. Evidence from gene trees, protein alignments, and diatom life history together suggest that habitat transitions were largely the product of homoplasy rather than hemiplasy, a condition where transitions occur on branches in gene trees not shared with the species tree. Nevertheless, we identified a set of putatively hemiplasious genes, many of which have been associated with shifts to low salinity, indicating that hemiplasy played a small but potentially important role in freshwater adaptation. Accounting for differences in evolutionary outcomes, in which some taxa became locked into freshwaters while others were able to return to the ocean or become salinity generalists, might help further distinguish different sources of adaptive mutation in freshwater diatoms. [hemiplasy; homoplasy; phylogenomics; salinity, Thalassiosirales.]

    more » « less
  4. Abstract

    The introduction and spread of non‐native species restructure native ecosystems and can be particularly impactful when invaders are ecosystem engineers or habitat‐forming species. In coastal, estuarine, and marine systems, submerged aquatic vegetation (SAV), like macroalgae and seagrasses, form key habitats for nekton, serving as nurseries, foraging grounds, and reproduction sites. If non‐native ecosystem engineers can provide sufficient structure and/or resources, they may exert a neutral or positive effect on organisms occupying higher trophic positions. As such, we hypothesized that nekton response to non‐native SAV species may be neutral or positive. We performed a quantitative meta‐analysis to quantify impacts of non‐native SAV on native crabs, fishes, and shrimps. We extracted data from 35 studies and evaluated 11 response metrics related to facilitation (e.g., habitat use and foraging), restricting our analysis to studies that compared at least one of these metrics in nekton from co‐occurring native and non‐native SAV habitats in marine, coastal, or estuarine systems. We found that nekton abundance, species richness, and biomass were the most assessed metrics of nekton performance. Our pooled data revealed differential results among response metrics, with nekton growth and reproduction enhanced in non‐native habitats and species richness enhanced in a native setting. The mean effect sizes for all other nekton response metrics, including abundance, had 95% CIs that overlapped zero, indicating no difference in response between native and non‐native SAV. For many endpoints, limited sample sizes prevented robust inferences, but they also highlighted areas where more research is needed in future studies. Non‐native species have the potential to restructure the systems they invade. Our results lend support to the relative trophic position hypothesis, indicating that non‐native habitat formers may facilitate native organisms in higher trophic levels. We identify research gaps that may guide future studies and allow for a more comprehensive understanding of responses to non‐native ecosystem engineers.

    more » « less
  5. Abstract

    Climate change is increasing the frequency, severity, and extent of wildfires and drought in many parts of the world, with numerous repercussions for the physical, chemical, and biological characteristics of streams. However, information on how these perturbations affect top predators and their impacts on lower trophic levels in streams is limited.

    The top aquatic predator in southern California streams is nativeOncorhynchus mykiss, the endangered southern California steelhead trout (trout). To examine relationships among the distribution of trout, environmental factors, and stream invertebrate resources and assemblages, we sampled pools in 25 stream reaches that differed in the presence (nine reaches) or absence (16 reaches) of trout over 12 years, including eight reaches where trout were extirpated during the study period by drought or post‐fire flood disturbances.

    Trout were present in deep pools with high water and habitat quality. Invertebrate communities in trout pools were dominated by a variety of medium‐sized collector–gatherer and shredder invertebrate taxa with non‐seasonal life cycles, whereas tadpoles and large, predatory invertebrates (Odonata, Coleoptera, Hemiptera [OCH]), often with atmospheric breather traits, were more abundant in troutless than trout pools.

    Structural equation modelling of the algal‐based food web indicated a trophic cascade from trout to predatory invertebrates to collector–gatherer taxa and weaker direct negative trout effects on grazers; however, both grazers and collector–gatherers also were positively related to macroalgal biomass. Structural equation modelling also suggested that bottom‐up interactions and abiotic factors drove the detritus‐based food web, with shredder abundance being positively related to leaf litter (coarse particulate organic matter) levels, which, in turn, were positively related to canopy cover and negatively related to flow. These results emphasise the context dependency of trout effects on prey communities and of the relative importance of top‐down versus bottom‐up interactions on food webs, contingent on environmental conditions (flow, light, nutrients, disturbances) and the abundances and traits of component taxa.

    Invertebrate assemblage structure changed from a trout to a troutless configuration within a year or two after trout were lost owing to post‐fire scouring flows or drought. Increases in OCH abundance after trout were lost were much more variable after drought than after fire. The reappearance of trout in one stream resulted in quick, severe reductions in OCH abundance.

    These results indicate that climate‐change induced disturbances can result in the extirpation of a top predator, with cascading repercussions for stream communities and food webs. This study also emphasises the importance of preserving or restoring refuge habitats, such as deep, shaded, perennial, cool stream pools with high habitat and water quality, to prevent the extirpation of sensitive species and preserve native biodiversity during a time of climate change.

    more » « less