skip to main content


Title: Estuarine gradients dictate spatiotemporal variations of microbiome networks in the Chesapeake Bay
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.

Results

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.

Conclusion

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
NSF-PAR ID:
10360457
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Springer Science + Business Media
Date Published:
Journal Name:
Environmental Microbiome
Volume:
16
Issue:
1
ISSN:
2524-6372
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Background

    Studying the co-occurrence network structure of microbial samples is one of the critical approaches to understanding the perplexing and delicate relationship between the microbe, host, and diseases. It is also critical to develop a tool for investigating co-occurrence networks and differential abundance analyses to reveal the disease-related taxa–taxa relationship. In addition, it is also necessary to tighten the co-occurrence network into smaller modules to increase the ability for functional annotation and interpretability of  these taxa-taxa relationships.  Also, it is critical to retain the phylogenetic relationship among the taxa to identify differential abundance patterns, which can be used to resolve contradicting functions reported by different studies.

    Results

    In this article, we present Correlation and Consensus-based Cross-taxonomy Network Analysis (C3NA), a user-friendly R package for investigating compositional microbial sequencing data to identify and compare co-occurrence patterns across different taxonomic levels. C3NA contains two interactive graphic user interfaces (Shiny applications), one of them dedicated to the comparison between two diagnoses, e.g., disease versus control. We used C3NA to analyze two well-studied diseases, colorectal cancer, and Crohn’s disease. We discovered clusters of study and disease-dependent taxa that overlap with known functional taxa studied by other discovery studies and differential abundance analyses.

    Conclusion

    C3NA offers a new microbial data analyses pipeline for refined and enriched taxa–taxa co-occurrence network analyses, and the usability was further expanded via the built-in Shiny applications for interactive investigation.

     
    more » « less
  2. Abstract

    Ecological factors contributing to depth-related diversification of marine Thaumarchaeota populations remain largely unresolved. To investigate the role of potential microbial associations in shaping thaumarchaeal ecotype diversification, we examined co-occurrence relationships in a community composition dataset (16S rRNA V4-V5 region) collected as part of a 2-year time series in coastal Monterey Bay. Ecotype groups previously defined based on functional gene diversity—water column A (WCA), water column B (WCB) and Nitrosopumilus-like clusters—were recovered in the thaumarchaeal 16S rRNA gene phylogeny. Networks systematically reflected depth-related patterns in the abundances of ecotype populations, suggesting thaumarchaeal ecotypes as keystone members of the microbial community below the euphotic zone. Differential environmental controls on the ecotype populations were further evident in subnetwork modules showing preferential co-occurrence of OTUs belonging to the same ecotype cluster. Correlated abundances of Thaumarchaeota and heterotrophic bacteria (e.g., Bacteroidetes, Marinimicrobia and Gammaproteobacteria) indicated potential reciprocal interactions via dissolved organic matter transformations. Notably, the networks recovered ecotype-specific associations between thaumarchaeal and Nitrospina OTUs. Even at depths where WCB-like Thaumarchaeota dominated, Nitrospina OTUs were found to preferentially co-occur with WCA-like and Nitrosopumilus-like thaumarchaeal OTUs, highlighting the need to investigate the ecological implications of the composition of nitrifier assemblages in marine waters.

     
    more » « less
  3. Abstract

    Blue crab (Callinectes sapidus) supports lucrative Mid‐Atlantic crustacean fisheries and plays an important role in estuarine ecology, so their larval transport and recruitment dynamics in the Maryland Coastal Bays system were investigated using simulated and observed surface drifters. Relative contributions of winds, tides, density gradients, and waves to larval recruitment success were identified during the spawning season, particularly under hurricane conditions in 2014. Based on temperature (e.g., 19–29°C) and salinity conditions (e.g., 23–33 PSU), particles representing virtual blue crab larvae were released into the model domain from early June to late October 2014. During the spawning season, variations in the larval recruitment success caused by wind speed and direction, tides (e.g., affecting through inlets), density gradients (e.g., salinity variations), and surface gravity waves were 17%, 4%, −9%, and 17%, respectively. During Hurricane Arthur (2014), variability of self‐recruitment success caused by density gradients are negligible while by other three factors are comparable at 3%–4%. Surface drifter experiments support the modeling results that larval recruitment success is strongly associated with the coastal circulation. The high (low) self‐recruitment success in the Assawoman and Chincoteague Bays (Sinepuxent Bay) is related to the locally weak (strong) circulation; released larvae escape from inlets are likely recruited to southern Fenwick and northern Assateague Islands, and the coastal regions outside the Chincoteague Inlet. Understanding physical factors influencing larval recruitment success helps resource managers make informed decisions about habitat restoration and harvest regulations, in addition to seafood‐related food security.

     
    more » « less
  4. Abstract

    The exchange between estuaries and the coastal ocean is a key dynamical driver impacting nutrient and phytoplankton concentrations and regulating estuarine residence time, hypoxia, and acidification. Estuarine exchange flows can be particularly challenging to monitor because many systems have strong vertical and lateral velocity shear and sharp gradients in water properties that vary over space and time, requiring high‐resolution measurements in order to accurately constrain the flux. The total exchange flow (TEF) method provides detailed information about the salinity structure of the exchange, but requires observations (or model resolution) that resolve the time and spatial co‐variability of salinity and currents. The goal of this analysis is to provide recommendations for measuring TEF with the most efficient spatial sampling resolution. Results from three realistic hydrodynamic models were investigated. These model domains included three estuary types: a bay (San Diego Bay), a salt‐wedge (Columbia River), and a fjord (Salish Sea). Model fields were sampled using three different mooring strategies, varying the number of mooring locations (lateral resolution) and sample depths (vertical resolution) with each method. The exchange volume transport was more sensitive than salinity to the sampling resolution. Most (>90%) of the exchange flow magnitude was captured by three to four moorings evenly distributed across the estuarine channel with a minimum threshold of 1–5 sample depths, which varied depending on the vertical stratification. These results can improve our ability to observe and monitor the exchange and transport of water masses efficiently with limited resources.

     
    more » « less
  5. Abstract

    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