Occurrence, Diversity, and Genomes of “Candidatus Patescibacteria” along the Early Diagenesis of Marine Sediments

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Author(s)Zhao, Rui
Author(s)Farag, Ibrahim F.
Author(s)Jørgensen, Steffen L.
Author(s)Biddle, Jennifer F.
Date Accessioned2023-02-10T15:02:04Z
Date Available2023-02-10T15:02:04Z
Publication Date2022-12-05
DescriptionThis article was originally published in Applied and Environmental Microbiology. The version of record is available at: https://doi.org/10.1128/aem.01409-22. This article will be embargoed until 06/05/2023.
AbstractThe phylum “Candidatus Patescibacteria” (or Candidate Phyla Radiation [CPR]) accounts for roughly one-quarter of microbial diversity on Earth, but the presence and diversity of these bacteria in marine sediments have been rarely charted. Here, we investigate the abundance, diversity, and metabolic capacities of CPR bacteria in three sediment sites (Mohns Ridge, North Pond, and Costa Rica Margin) with samples covering a wide range of redox zones formed during the early diagenesis of organic matter. Through metagenome sequencing, we found that all investigated sediment horizons contain “Ca. Patescibacteria” (0.4 to 28% of the total communities), which are affiliated with the classes “Ca. Paceibacteria,” “Ca. Gracilibacteria,” “Ca. Microgenomatia,” “Ca. Saccharimonadia,” “Ca. ABY1,” and “Ca. WWE3.” However, only a subset of the diversity of marine sediment “Ca. Patescibacteria,” especially the classes “Ca. Paceibacteria” and “Ca. Gracilibacteria,” can be captured by 16S rRNA gene amplicon sequencing with commonly used universal primers. We recovered 11 metagenome-assembled genomes (MAGs) of CPR from these sediments, most of which are novel at the family or genus level in the “Ca. Paceibacteria” class and are missed by the amplicon sequencing. While individual MAGs are confined to specific anoxic niches, the lack of capacities to utilize the prevailing terminal electron acceptors indicates that they may not be directly selected by the local redox conditions. These CPR bacteria lack essential biosynthesis pathways and may use a truncated glycolysis pathway to conserve energy as fermentative organotrophs. Our findings suggest that marine sediments harbor some novel yet widespread CPR bacteria during the early diagenesis of organic matter, which needs to be considered in population dynamics assessments in this vast environment. IMPORTANCE Ultrasmall-celled “Ca. Patescibacteria” have been estimated to account for one-quarter of the total microbial diversity on Earth, the parasitic lifestyle of which may exert a profound control on the overall microbial population size of the local ecosystems. However, their diversity and metabolic functions in marine sediments, one of the largest yet understudied ecosystems on Earth, remain virtually uncharacterized. By applying cultivation-independent approaches to a range of sediment redox zones, we reveal that “Ca. Patescibacteria” members are rare but widespread regardless of the prevailing geochemical conditions. These bacteria are affiliated with novel branches of “Ca. Patescibacteria” and have been largely missed in marker gene-based surveys. They do not have respiration capacity but may conserve energy by fermenting organic compounds from their episymbiotic hosts. Our findings suggest that these novel “Ca. Patescibacteria” are among the previously overlooked microbes in diverse marine sediments.
SponsorComputational support from the University of Delaware Center for Bioinformatics and Computational Biology Core Facility and the use of the BIOMIX compute cluster were made possible through funding from Delaware INBRE (NIGMS P20GM103446), the State of Delaware, and the Delaware Biotechnology Institute. This work was funded by the K. G. Jebsen Foundation and the Trond Mohns Science Foundation (to S.L.J.). R.Z. and J.F.B. were funded in part by the W. M. Keck Foundation.
CitationZhao, Rui, Ibrahim F. Farag, Steffen L. Jørgensen, and Jennifer F. Biddle. “Occurrence, Diversity, and Genomes of "Candidatus Patescibacteria” along the Early Diagenesis of Marine Sediments.” Edited by Jennifer B. Glass. Applied and Environmental Microbiology 88, no. 24 (December 5, 2022): e01409-22. https://doi.org/10.1128/aem.01409-22.
ISSN1098-5336
URLhttps://udspace.udel.edu/handle/19716/32264
Languageen_US
PublisherApplied and Environmental Microbiology
Keywordsmarine sediments
Keywordsearly diagenesis
KeywordsPatescibacteria
Keywordsredox zones
KeywordsCandidate Phyla Radiation
Keywordsbiogeochemistry
Keywordsmetagenome
TitleOccurrence, Diversity, and Genomes of “Candidatus Patescibacteria” along the Early Diagenesis of Marine Sediments
TypeArticle
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