Archaeal ecology and archaea involved in biodeterioration of stone monuments

Abstract

The Archaea, as a newly established life domain distinguished from the Bacteria and Eukarya, has been expanded from its initial two phyla to the current 24-28 phyla. This rapid development has greatly enriched our knowledge of the evolution of life. Benefiting from the revolution of the high throughput sequencing technologies and the bioinformatics progress for assemble of metagenomics and genomics, many novel archaeal lineages and genomes have been discovered from many environments, revealing an important ecological role of archaea on Earth. Estuary harbors a huge number of microorganisms, but the ecological patterns of archaea in this ecosystem are still unclear, especially for the archaeal DPANN superphylum. In addition, some archaeal lineages, such as ammonia-oxidizing archaea (AOA) and halophilic archaea, are detected to be abundant on the deteriorating stone monuments of the world cultural heritage, but their potential roles in the biodeterioration of stone monuments remain unknown largely. In this study, an investigation was carried out to delineate the global distribution patterns and the ecological roles of Woesearchaeota of the DPANN superphylum, and also unveil the contribution of archaeal lineages together with other microorganisms to the biodeterioration of stone monuments. A high biodiversity of archaea, increasing from the high-latitude estuaries to the lower ones, was observed in global estuarine ecosystems. Phylogenetic analysis revealed that estuarine ecosystems contain more than 12 phyla dominated by Bathyarchaeota, Euryarchaeota and Thaumarchaeota. Interestingly, archaeal distribution is probably driven by latitude. Phylogenetic-based analyses showed that high diversity of Woesearchaeota with 26 subgroups (at class level) is widely distributed in continental anaerobic environments and that oxic status would be a crucial factor affecting the patterns of ecology and evolution. The presence of ferredoxin-dependent biochemical pathways suggested a selection for distribution to biotopes and an adaptive strategy for selection from anoxic to oxic environments. Metabolic prediction and modeling supported an anaerobic heterotrophic lifestyle and a potential syntrophy of Woesearchaeota and methanogens. The findings provide a framework of ecology and evolution for Woesearchaeota. Moreover, ecological patterns and genomic analyses revealed the potential roles of Woesearchaeota in anaerobic biogeochemical cycling of carbon, nitrogen, and sulfur. Lastly, archaeal contribution to biodeterioration of stone monuments was also discussed and the significance of water management and control was highlighted in the conservation of the world cultural heritage. Archaea are a promising group for discovery of their lifestyle and contribution to the biochemical processes in ecosystems.