Planktonic/benthic Bathyarchaeota as a "gatekeeper" enhance archaeal nonrandom co-existence and deterministic...

Archaea, the third proposed domain of life, mediate carbon and nutrient cycling in global natural habitats. Compared with bacteria, our knowledge about archaeal ecological modes in large freshwater environments subject to varying natural and human factors is limited. By metabarcoding analysis of 303 samples, we provided the first integrate biogeography about archaeal compositions, co-existence networks, and assembling processes within a 6000 km continuum of the Yangtze River. Our study revealed that, among the major phyla, water samples owned a higher proportion of Thaumarchaeota (62.8%), while sediments had higher proportions of Euryarchaeota (33.4%) and Bathyarchaeota (18.8%). A decline of polarization in phylum abundance profile was observed from plateau/mountain/hill to basin/plain areas, which was attributed to the increase of nutrients and metals. Planktonic and benthic Bathyarchaeota tended to co-occur with both major (e.g., methanogens or Thermoplasmata) and minor (e.g., Asgard or DPANN) taxa in the non-random networks, harboring the highest richness and abundances of keystone species and contributing the most positively to edge number, node degree, and nearest neighbor degree. Furthermore, we noted significantly positive contributions of Bathyarchaeota abundance and network complexity to the dominance of deterministic process in archaeal assembly (water: 65.3%; sediments: 92.6%), since higher carbon metabolic versatility of Bathyarchaeota would benefit archaeal symbiotic relations. Stronger deterministic assembling was identified at the lower-reach plain, and higher concentrations of ammonium and aluminum separately functioning as nutrition and agglomerator were the main environmental drivers. We lastly found that the Three Gorges Dam caused a simultaneous drop of benthic Bathyarchaeota abundance, network co-existence, and deterministic effects immediately downstream due to riverbed erosion as a local interference. These findings highlight that Bathyarchaeota are a "gatekeeper" to promote fluvial archaeal diversity, stability, and predictability under varying macroscopic and microscopic factors, expanding our knowledge about microbial ecology in freshwater biogeochemical cycling globally.