skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Phenotypic Comparability from Genotypic Variability among Physically Structured Microbial Consortia
Abstract Microbiomes represent the collective bacteria, archaea, protist, fungi, and virus communities living in or on individual organisms that are typically multicellular eukaryotes. Such consortia have become recognized as having significant impacts on the development, health, and disease status of their hosts. Since understanding the mechanistic connections between an individual’s genetic makeup and their complete set of traits (i.e., genome to phenome) requires consideration at different levels of biological organization, this should include interactions with, and the organization of, microbial consortia. To understand microbial consortia organization, we elucidated the genetic constituents among phenotypically similar (and hypothesized functionally-analogous) layers (i.e., top orange, second orange, pink, and green layers) in the unique laminated orange cyanobacterial–bacterial crusts endemic to Hawaii’s anchialine ecosystem. High-throughput amplicon sequencing of ribosomal RNA hypervariable regions (i.e., Bacteria-specific V6 and Eukarya-biased V9) revealed microbial richness increasing by crust layer depth, with samples of a given layer more similar to different layers from the same geographic site than to their phenotypically-analogous layer from different sites. Furthermore, samples from sites on the same island were more similar to each other, regardless of which layer they originated from, than to analogous layers from another island. However, cyanobacterial and algal taxa were abundant in all surface and bottom layers, with anaerobic and chemoautotrophic taxa concentrated in the middle two layers, suggesting crust oxygenation from both above and below. Thus, the arrangement of oxygenated vs. anoxygenated niches in these orange crusts is functionally distinct relative to other laminated cyanobacterial–bacterial communities examined to date, with convergent evolution due to similar environmental conditions a likely driver for these phenotypically comparable but genetically distinct microbial consortia.  more » « less
Award ID(s):
1927470
PAR ID:
10196253
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
Integrative and Comparative Biology
Volume:
60
Issue:
2
ISSN:
1540-7063
Page Range / eLocation ID:
288 to 303
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Animals often shape environmental microbial communities, which can in turn influence animal gut microbiomes. Invasive species in critical habitats may reduce grazing pressure from native species and shift microbial communities. The landlocked coastal ponds, pools, and caves that make up the Hawaiian anchialine ecosystem support an endemic shrimp (Halocaridina rubra) that grazes on diverse benthic microbial communities, including orange cyanobacterial‐bacterial crusts and green algal mats. Here, we asked how shrimp: (1) shape the abundance and composition of microbial communities, (2) respond to invasive fishes, and (3) whether their gut microbiomes are affected by environmental microbial communities. We demonstrate that ecologically relevant levels of shrimp grazing significantly reduce epilithon biomass. Shrimp grazed readily and grew well on both orange crusts and green mat communities. However, individuals from orange crusts were larger, despite crusts having reduced concentrations of key fatty acids. DNA profiling revealed shrimp harbor a resident gut microbiome distinct from the environment, which is relatively simple and stable across space (including habitats with different microbial communities) and time (between wild‐caught individuals and those maintained in the laboratory for >2 yr). DNA profiling also suggests shrimp grazing alters environmental microbial community composition, possibly through selective consumption and/or physical interactions. While this work suggests grazing by endemic shrimp plays a key role in shaping microbial communities in the Hawaiian anchialine ecosystem, the hypothesized drastic ecological shifts resulting from invasive fishes may be an oversimplification as shrimp may largely avoid predation. Moreover, environmental microbial communities may have little influence on shrimp gut microbiomes. 
    more » « less
  2. Abstract Determining the repertoire of a microbe's molecular functions is a central question in microbial biology. Modern techniques achieve this goal by comparing microbial genetic material against reference databases of functionally annotated genes/proteins or known taxonomic markers such as 16S rRNA. Here, we describe a novel approach to exploring bacterial functional repertoires without reference databases. Our Fusion scheme establishes functional relationships between bacteria and assigns organisms to Fusion-taxa that differ from otherwise defined taxonomic clades. Three key findings of our work stand out. First, bacterial functional comparisons outperform marker genes in assigning taxonomic clades. Fusion profiles are also better for this task than other functional annotation schemes. Second, Fusion-taxa are robust to addition of novel organisms and are, arguably, able to capture the environment-driven bacterial diversity. Finally, our alignment-free nucleic acid-based Siamese Neural Network model, created using Fusion functions, enables finding shared functionality of very distant, possibly structurally different, microbial homologs. Our work can thus help annotate functional repertoires of bacterial organisms and further guide our understanding of microbial communities. 
    more » « less
  3. Abstract Background Mosses in high-latitude ecosystems harbor diverse bacterial taxa, including N 2 -fixers which are key contributors to nitrogen dynamics in these systems. Yet the relative importance of moss host species, and environmental factors, in structuring these microbial communities and their N 2 -fixing potential remains unclear. We studied 26 boreal and tundra moss species across 24 sites in Alaska, USA, from 61 to 69° N. We used cultivation-independent approaches to characterize the variation in moss-associated bacterial communities as a function of host species identity and site characteristics. We also measured N 2 -fixation rates via 15 N 2 isotopic enrichment and identified potential N 2 -fixing bacteria using available literature and genomic information. Results Host species identity and host evolutionary history were both highly predictive of moss microbiome composition, highlighting strong phylogenetic coherence in these microbial communities. Although less important, light availability and temperature also influenced composition of the moss microbiome. Finally, we identified putative N 2 -fixing bacteria specific to some moss hosts, including potential N 2 -fixing bacteria outside well-studied cyanobacterial clades. Conclusions The strong effect of host identity on moss-associated bacterial communities demonstrates mosses’ utility for understanding plant-microbe interactions in non-leguminous systems. Our work also highlights the likely importance of novel bacterial taxa to N 2 -fixation in high-latitude ecosystems. 
    more » « less
  4. Cycles of nutrients (N, P, etc.) and resources (C) are a defining emergent feature of ecosystems. Cycling plays a critical role in determining ecosystem structure at all scales, from microbial communities to the entire biosphere. Stable cycles are essential for ecosystem persistence because they allow resources and nutrients to be regenerated. Therefore, a central problem in ecology is understanding how ecosystems are organized to sustain robust cycles. Addressing this problem quantitatively has proved challenging because of the difficulties associated with manipulating ecosystem structure while measuring cycling. We address this problem using closed microbial ecosystems (CES), hermetically sealed microbial consortia provided with only light. We develop a technique for quantifying carbon cycling in hermetically sealed microbial communities and show that CES composed of an alga and diverse bacterial consortia self-organize to robustly cycle carbon for months. Comparing replicates of diverse CES, we find that carbon cycling does not depend strongly on the taxonomy of the bacteria present. Moreover, despite strong taxonomic differences, self-organized CES exhibit a conserved set of metabolic capabilities. Therefore, an emergent carbon cycle enforces metabolic but not taxonomic constraints on ecosystem organization. Our study helps establish closed microbial communities as model ecosystems to study emergent function and persistence in replicate systems while controlling community composition and the environment. 
    more » « less
  5. Symbiotic interactions between fungi and bacteria range from positive to negative. They are ubiquitous in free-living as well as host-associated microbial communities worldwide. Yet, the impact of fungal-bacterial symbioses on the organization and dynamics of microbial communities is uncertain. There are two reasons for this uncertainty: (1) knowledge gaps in the understanding of the genetic mechanisms underpinning fungal-bacterial symbioses and (2) prevailing interpretations of ecological theory that favor antagonistic interactions as drivers stabilizing biological communities despite the existence of models emphasizing contributions of positive interactions. This review synthesizes information on fungal-bacterial symbioses common in the free-living microbial communities of the soil as well as in host-associated polymicrobial biofilms. The interdomain partnerships are considered in the context of the relevant community ecology models, which are discussed critically. 
    more » « less