Microscopic and metatranscriptomic analyses revealed unique cross-domain parasitism between phylum
Candidatus
Patescibacteria/candidate phyla radiation and methanogenic archaea in anaerobic ecosystems
ABSTRACT
To verify whether members of the phylum
Candidatus
Patescibacteria parasitize archaea, we applied cultivation, microscopy, metatranscriptomic, and protein structure prediction analyses on the Patescibacteria-enriched cultures derived from a methanogenic bioreactor. Amendment of cultures with exogenous methanogenic archaea, acetate, amino acids, and nucleoside monophosphates increased the relative abundance of
Ca
. Patescibacteria. The predominant
Ca
. Patescibacteria were families
Ca
. Yanofskyibacteriaceae and
Ca
. Minisyncoccaceae, and the former showed positive linear relationships (
r
2
≥ 0.70)
Methanothrix
in their relative abundances, suggesting related growth patterns.
Methanothrix
and
Methanospirillum
cells with attached
Ca
. Yanofskyibacteriaceae and
Ca
. Minisyncoccaceae, respectively, had significantly lower cellular activity than those of the methanogens without
Ca
. Patescibacteria, as extrapolated from fluorescence
in situ
hybridization-based fluorescence. We also observed that parasitized methanogens often had cell surface deformations. Some
Methanothrix
-like filamentous cells were dented where the submicron cells were attached.
Ca
. Yanofskyibacteriaceae and
Ca
. Minisyncoccaceae highly expressed extracellular enzymes, and based on structural predictions, some contained peptidoglycan-binding domains with potential involvement in host cell attachment. Collectively, we propose that the interactions of
Ca
. Yanofskyibacteriaceae and
Ca
. Minisyncoccaceae with methanogenic archaea are parasitisms.
IMPORTANCE
Culture-independent DNA sequencing approaches have explored diverse yet-to-be-cultured microorganisms and have significantly expanded the tree of life in recent years. One major lineage of the domain Bacteria,
Ca
. Patescibacteria (also known as candidate phyla radiation), is widely distributed in natural and engineered ecosystems and has been thought to be dependent on host bacteria due to the lack of several biosynthetic pathways and small cell/genome size. Although bacteria-parasitizing or bacteria-preying
Ca
. Patescibacteria have been described, our recent studies revealed that some lineages can specifically interact with archaea. In this study, we provide strong evidence that the relationship is parasitic, shedding light on overlooked roles of
Ca
. Patescibacteria in anaerobic habitats.