skip to main content


Title: Differential co-occurrence relationships shaping ecotype diversification within Thaumarchaeota populations in the coastal ocean water column
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
NSF-PAR ID:
10485645
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
The ISME Journal
Volume:
13
Issue:
5
ISSN:
1751-7362
Format(s):
Medium: X Size: p. 1144-1158
Size(s):
p. 1144-1158
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Nitrification plays a key role in marine ecosystems whereThaumarchaeotaare thought to be responsible for most of the ammonia oxidation in the water column. Over a 2‐yr, near‐monthly time series at two sites in Monterey Bay we observed repeatable seasonal and depth‐based patterns ofThaumarchaeotaecotype abundance that highlighted a clear delineation between populations in shallow euphotic (< 50 m) vs. deeper mesopelagic (60–500 m) depths. Euphotic depths show greater seasonality and influence from light, while mesopelagic waters have trends based on water mass and other covarying features with depth. Three major ecotypes were recovered: aNitrosopumilus‐like (NP) group, aNitrosopelagicus‐like ecotype containing “shallow” water column A (WCA) members, and an ecotype affiliated with the “deep” water column B (WCB)Thaumarchaeota. These ecotypes show a strong depth distribution, with WCB dominant at ≥ 200 m depth and WCA most abundant in surface (5–100 m) waters. The NP ecotype was found throughout the water column with the highest abundance in summer, and was the only ecotype showing a correlation with measured nitrification rates. We also found three abundant taxa related toNitrospina—the major nitrite‐oxidizing bacteria in the ocean; these showed clear connections to each of the threeThaumarchaeotaecotypes, suggesting a specific relationship between both steps of nitrification. Our results support the importance of ecotype‐based analysis ofThaumarchaeotaand show that their abundance and distribution are controlled based on their water column position, with a distinct shift at 50 m between euphotic and mesopelagic depths.

     
    more » « less
  2. Summary

    Ammonia‐oxidizing archaea (AOA) of the phylumThaumarchaeotaare key players in nutrient cycling, yet large gaps remain in our understanding of their ecology and metabolism. Despite multiple lines of evidence pointing to a central role for copper‐containing nitrite reductase (NirK) in AOA metabolism, the thaumarchaealnirKgene is rarely studied in the environment. In this study, we examine the diversity ofnirKin the marine pelagic environment, in light of previously described ecological patterns of pelagic thaumarchaeal populations. Phylogenetic analyses show thatnirKbetter resolves diversification patterns of marineThaumarchaeota, compared to the conventionally used marker geneamoA. Specifically, we demonstrate that the three major phylogenetic clusters of marinenirKcorrespond to the three ‘ecotype’ populations of pelagicThaumarchaeota. In this context, we further examine the relative distributions of the three variant groups in metagenomes and metatranscriptomes representing two depth profiles in coastal Monterey Bay. Our results reveal thatnirKeffectively tracks the dynamics of thaumarchaeal ecotype populations, particularly finer‐scale diversification patterns within major lineages. We also find evidence for multiple copies ofnirKper genome in a fraction of thaumarchaeal cells in the water column, which must be taken into account when using it as a molecular marker.

     
    more » « less
  3. Methane seep systems along continental margins host diverse and dynamic microbial assemblages, sustained in large part through the microbially mediated process of sulfate-coupled Anaerobic Oxidation of Methane (AOM). This methanotrophic metabolism has been linked to consortia of anaerobic methane-oxidizing archaea (ANME) and sulfate-reducing bacteria (SRB). These two groups are the focus of numerous studies; however, less is known about the wide diversity of other seep associated microorganisms. We selected a hierarchical set of FISH probes targeting a range ofDeltaproteobacteriadiversity. Using the Magneto-FISH enrichment technique, we then magnetically captured CARD-FISH hybridized cells and their physically associated microorganisms from a methane seep sediment incubation. DNA from nested Magneto-FISH experiments was analyzed using Illumina tag 16S rRNA gene sequencing (iTag). Enrichment success and potential bias with iTag was evaluated in the context of full-length 16S rRNA gene clone libraries, CARD-FISH, functional gene clone libraries, and iTag mock communities. We determined commonly used Earth Microbiome Project (EMP) iTAG primers introduced bias in some common methane seep microbial taxa that reduced the ability to directly compare OTU relative abundances within a sample, but comparison of relative abundances between samples (in nearly all cases) and whole community-based analyses were robust. The iTag dataset was subjected to statistical co-occurrence measures of the most abundant OTUs to determine which taxa in this dataset were most correlated across all samples. Many non-canonical microbial partnerships were statistically significant in our co-occurrence network analysis, most of which were not recovered with conventional clone library sequencing, demonstrating the utility of combining Magneto-FISH and iTag sequencing methods for hypothesis generation of associations within complex microbial communities. Network analysis pointed to many co-occurrences containing putatively heterotrophic, candidate phyla such as OD1,Atribacteria, MBG-B, and Hyd24-12 and the potential for complex sulfur cycling involvingEpsilon-,Delta-, andGammaproteobacteriain methane seep ecosystems.

     
    more » « less
  4. Abstract

    Lake Lanier (Georgia, USA) is home to more than 11,000 microbial Operational Taxonomic Units (OTUs), many of which exhibit clear annual abundance patterns. To assess the dynamics of this microbial community, we collected time series data of 16S and 18S rRNA gene sequences, recovered from 29 planktonic shotgun metagenomic datasets. Based on these data, we constructed a dynamic mathematical model of bacterial interactions in the lake and used it to analyze changes in the abundances of OTUs. The model accounts for interactions among 14 sub-communities (SCs), which are composed of OTUs blooming at the same time of the year, and three environmental factors. It captures the seasonal variations in abundances of the SCs quite well. Simulation results suggest that changes in water temperature affect the various SCs differentially and that the timing of perturbations is critical. We compared the model results with published results from Lake Mendota (Wisconsin, USA). These comparative analyses between lakes in two very different geographical locations revealed substantially more cooperation and less competition among species in the warmer Lake Lanier than in Lake Mendota.

     
    more » « less
  5. Weinert, Emily (Ed.)
    ABSTRACT When the oligotrophic microbial community was amended with Synechococcus -derived dissolved organic matter (SDOM) and incubated under the dark condition, archaea relative abundance was initially very low but made up more than 60% of the prokaryotic community on day 60, and remained dominant for at least 9 months. The archaeal sequences were dominated by Candidatus Nitrosopumilus , the Group I.1a Thaumarchaeota. The increase of Thaumarchaeota in the dark incubation corresponded to the period of delayed ammonium oxidation upon an initially steady increase in ammonia, supporting the remarkable competency of Thaumarchaeota in energy utilization and fixation of inorganic carbon in the ocean. IMPORTANCE Thaumarchaeota, which are ammonia-oxidizing archaea (AOA), are mainly chemolithoautotrophs that can fix inorganic carbon to produce organic matter in the dark. Their distinctive physiological traits and high abundance in the water column indicate the significant ecological roles they play in the open ocean. In our study, we found predominant Thaumarchaeota in the microbial community amended with cyanobacteria-derived lysate under the dark condition. Furthermore, Thaumarchaeota remained dominant in the microbial community even after 1 year of incubation. Through the ammonification process, dissolved organic matter (DOM) from cyanobacterial lysate was converted to ammonium which was used as an energy source for Thaumarchaeota to fix inorganic carbon into biomass. Our study further advocates the important roles of Thaumarchaeota in the ocean’s biogeochemical cycle. 
    more » « less