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

The 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. 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.

Automated summary

This study investigated the abundance, diversity, and metabolic capacities of CPR bacteria in marine sediments, finding a wide distribution and rich diversity of these bacteria compared to existing marker gene surveys. Through metagenome sequencing, the importance of these bacteria in sediments and their potential role in the early diagenesis of organic matter were revealed.