Unraveling the habitat preferences, ecological drivers, potential hosts, and auxiliary metabolism of soil giant viruses across China.

BACKGROUND: Soil giant viruses are increasingly believed to have profound effects on ecological functioning by infecting diverse eukaryotes. However, their biogeography and ecology remain poorly understood. RESULTS: In this study, we analyzed 333 soil metagenomes from 5 habitat types (farmland, forest, grassland, Gobi desert, and mine wasteland) across China and identified 533 distinct giant virus phylotypes affiliated with nine families, thereby greatly expanding the diversity of soil giant viruses. Among the nine families, Pithoviridae were the most diverse. The majority of phylotypes exhibited a heterogeneous distribution among habitat types, with a remarkably high proportion of unique phylotypes in mine wasteland. The abundances of phylotypes were negatively correlated with their environmental ranges. A total of 76 phylotypes recovered in this study were detectable in a published global topsoil metagenome dataset. Among climatic, geographical, edaphic, and biotic characteristics, soil eukaryotes were identified as the most important driver of beta-diversity of giant viral communities across habitat types. Moreover, co-occurrence network analysis revealed some pairings between giant viral phylotypes and eukaryotes (protozoa, fungi, and algae). Analysis of 44 medium- to high-quality giant virus genomes recovered from our metagenomes uncovered not only their highly shared functions but also their novel auxiliary metabolic genes related to carbon, sulfur, and phosphorus cycling. CONCLUSIONS: These findings extend our knowledge of diversity, habitat preferences, ecological drivers, potential hosts, and auxiliary metabolism of soil giant viruses. Video Abstract.

Eco-evolutionary dynamics of gut phageome in wild gibbons (Hoolock tianxing) with seasonal diet variations.

It has been extensively studied that the gut microbiome provides animals flexibility to adapt to food variability. Yet, how gut phageome responds to diet variation of wild animals remains unexplored. Here, we analyze the eco-evolutionary dynamics of gut phageome in six wild gibbons (Hoolock tianxing) by collecting individually-resolved fresh fecal samples and parallel feeding behavior data for 15 consecutive months. Application of complementary viral and microbial metagenomics recovers 39,198 virulent and temperate phage genomes from the feces. Hierarchical cluster analyses show remarkable seasonal diet variations in gibbons. From high-fruit to high-leaf feeding period, the abundances of phage populations are seasonally fluctuated, especially driven by the increased abundance of virulent phages that kill the Lachnospiraceae hosts, and a decreased abundance of temperate phages that piggyback the Bacteroidaceae hosts. Functional profiling reveals an enrichment through horizontal gene transfers of toxin-antitoxin genes on temperate phage genomes in high-leaf season, potentially conferring benefits to their prokaryotic hosts. The phage-host ecological dynamics are driven by the coevolutionary processes which select for tail fiber and DNA primase genes on virulent and temperate phage genomes, respectively. Our results highlight complex phageome-microbiome interactions as a key feature of the gibbon gut microbial ecosystem responding to the seasonal diet.

Gut microbiome responds compositionally and functionally to the seasonal diet variations in wild gibbons.

Wild animals may encounter multiple challenges especially food shortage and altered diet composition in their suboptimal ranges. Yet, how the gut microbiome responds to dietary changes remains poorly understood. Prior studies on wild animal microbiomes have typically leaned upon relatively coarse dietary records and individually unresolved fecal samples. Here, we conducted a longitudinal study integrating 514 time-series individually recognized fecal samples with parallel fine-grained dietary data from two Skywalker hoolock gibbon (Hoolock tianxing) groups populating high-altitude mountainous forests in western Yunnan Province, China. 16S rRNA gene amplicon sequencing showed a remarkable seasonal fluctuation in the gibbons' gut microbial community structure both across individuals and between the social groups, especially driven by the relative abundances of Lanchnospiraceae and Oscillospiraceae associated with fluctuating consumption of leaf. Metagenomic functional profiling revealed that diverse metabolisms associated with cellulose degradation and short-chain fatty acids (SCFAs) production were enriched in the high-leaf periods possibly to compensate for energy intake. Genome-resolved metagenomics further enabled the resolving metabolic capacities associated with carbohydrate breakdown among community members which exhibited a high degree of functional redundancy. Our results highlight a taxonomically and functionally sensitive gut microbiome actively responding to the seasonally shifting diet, facilitating the survival and reproduction of the endangered gibbon species in their suboptimal habitats.

Gut microbiota of skywalker hoolock gibbons (Hoolock tianxing) from different habitats and in captivity: Implications for gibbon health.

The gut microbiota plays an integral role in the metabolism and immunity of animal hosts, and provides insights into the health and habitat assessment of threatened animals. The skywalker hoolock gibbon (Hoolock tianxing) is a newly described gibbon species, and is considered an endangered species. Here, we used 16S rRNA amplicon sequencing to describe the fecal bacterial community of skywalker hoolock gibbons from different habitats and in captivity. Fecal samples (n = 5) from two captive gibbons were compared with wild populations (N = 6 gibbons, n = 33 samples). At the phylum level, Spirochetes, Proteobacteria, Firmicutes, Bacteroidetes dominated in captive gibbons, while Firmicutes, Bacteroidetes, and Tenericutes dominated in wild gibbons. At the genus level, captive gibbons were dominated by Treponema-2, followed by Succinivibrio and Cerasicoccus, while wild gibbons were dominated by Anaeroplasma, Prevotellaceae UCG-001, and Erysipelotrichaceae UCG-004. Captive rearing was significantly associated with lower taxonomic alpha-diversity, and different relative abundance of some dominant bacteria compared to wild gibbons. Predicted Kyoto Encyclopedia of Genes and Genomes pathway analyses showed that captive gibbons have significantly lower total pathway diversity and higher relative abundance of bacterial functions involved in "drug resistance: antimicrobial" and "carbohydrate metabolism" than wild gibbons. This study reveals the potential influence of captivity and habitat on the gut bacterial community of gibbons and provides a basis for guiding the conservation management of captive populations.

Microbial biogeography of acid mine drainage sediments at a regional scale across southern China.

Investigations of microbial biogeography in extreme environments provide unique opportunities to disentangle the roles of environment and space in microbial community assembly. Here, we reported a comprehensive microbial biogeographic survey of 90 acid mine drainage (AMD) sediment samples from 18 mining sites of various mineral types across southern China. We found that environmental selection was strong in determining the AMD habitat species pool. However, microbial alpha diversity was primarily explained by mining sites rather than environmental factors, and microbial beta diversity correlated more strongly with geographic than environmental distance at both large and small spatial scales. Particularly, the presence/absence of widespread AMD habitat generalists was only correlated with geographic distance and independent of environmental variation. These distance-decay patterns suggested that spatial processes played a more important role in determining microbial compositional variation across space; which could be explained by the reinforced impacts of dispersal limitation in less fluid, spatially structured sediment habitat with diverse pre-existing communities. In summary, our findings suggested that the deterministic assembling and spatial constraints interact to shape microbial biogeography in AMD sediments; and provided implications that spatial processes should be considered when predicting microbial dynamics in response to severe environmental change across large spatial scales.

Genomic Insights into the Ecological Role and Evolution of a Novel Thermoplasmata Order, "Candidatus Sysuiplasmatales".

Recent omics studies have provided invaluable insights into the metabolic potential, adaptation, and evolution of novel archaeal lineages from a variety of extreme environments. We utilized a genome-resolved metagenomic approach to recover eight medium- to high-quality metagenome-assembled genomes (MAGs) that likely represent a new order ("Candidatus Sysuiplasmatales") in the class Thermoplasmata from mine tailings and acid mine drainage (AMD) sediments sampled from two copper mines in South China. 16S rRNA gene-based analyses revealed a narrow habitat range for these uncultured archaea limited to AMD and hot spring-related environments. Metabolic reconstruction indicated a facultatively anaerobic heterotrophic lifestyle. This may allow the archaea to adapt to oxygen fluctuations and is thus in marked contrast to the majority of lineages in the domain Archaea, which typically show obligately anaerobic metabolisms. Notably, "Ca. Sysuiplasmatales" could conserve energy through degradation of fatty acids, amino acid metabolism, and oxidation of reduced inorganic sulfur compounds (RISCs), suggesting that they may contribute to acid generation in the extreme mine environments. Unlike the closely related orders Methanomassiliicoccales and "Candidatus Gimiplasmatales," "Ca. Sysuiplasmatales" lacks the capacity to perform methanogenesis and carbon fixation. Ancestral state reconstruction indicated that "Ca. Sysuiplasmatales," the closely related orders Methanomassiliicoccales and "Ca. Gimiplasmatales," and the orders SG8-5 and RBG-16-68-12 originated from a facultatively anaerobic ancestor capable of carbon fixation via the bacterial-type H4F Wood-Ljungdahl pathway (WLP). Their metabolic divergence might be attributed to different evolutionary paths. IMPORTANCE A wide array of archaea populate Earth's extreme environments; therefore, they may play important roles in mediating biogeochemical processes such as iron and sulfur cycling. However, our knowledge of archaeal biology and evolution is still limited, since the majority of the archaeal diversity is uncultured. For instance, most order-level lineages except Thermoplasmatales, Aciduliprofundales, and Methanomassiliicoccales within Thermoplasmata do not have cultured representatives. Here, we report the discovery and genomic characterization of a novel order, "Ca. Sysuiplasmatales," within Thermoplasmata in extremely acidic mine environments. "Ca. Sysuiplasmatales" are inferred to be facultatively anaerobic heterotrophs and likely contribute to acid generation through the oxidation of RISCs. The physiological divergence between "Ca. Sysuiplasmatales" and closely related Thermoplasmata lineages may be attributed to different evolutionary paths. These results expand our knowledge of archaea in the extreme mine ecosystem.

Depth-related variability in viral communities in highly stratified sulfidic mine tailings.

BACKGROUND: Recent studies have significantly expanded our knowledge of viral diversity and functions in the environment. Exploring the ecological relationships between viruses, hosts, and the environment is a crucial first step towards a deeper understanding of the complex and dynamic interplays among them. RESULTS: Here, we obtained extensive 16S rRNA gene amplicon, metagenomics sequencing, and geochemical datasets from different depths of two highly stratified sulfidic mine tailings cores with steep geochemical gradients especially pH, and explored how variations in viral community composition and functions were coupled to the co-existing prokaryotic assemblages and the varying environmental conditions. Our data showed that many viruses in the mine tailings represented novel genera, based on gene-sharing networks. Siphoviridae, Podoviridae, and Myoviridae dominated the classified viruses in the surface tailings and deeper layers. Both viral richness and normalized coverage increased with depth in the tailings cores and were significantly correlated with geochemical properties, for example, pH. Viral richness was also coupled to prokaryotic richness (Pearson's r = 0.65, P = 0.032). The enrichment of prophages in the surface mine tailings suggested a preference of lysogenic viral lifestyle in more acidic conditions. Community-wide comparative analyses clearly showed that viruses in the surface tailings encoded genes mostly with unknown functions while viruses in the deeper layers contained genes mainly annotated as conventional functions related to metabolism and structure. Notably, significantly abundant assimilatory sulfate reduction genes were identified from the deeper tailings layers and they were widespread in viruses predicted to infect diverse bacterial phyla. CONCLUSIONS: Overall, our results revealed a depth-related distribution of viral populations in the extreme and heterogeneous tailings system. The viruses may interact with diverse hosts and dynamic environmental conditions and likely play a role in the functioning of microbial community and modulate sulfur cycles in situ. Video Abstract.

A simple slash-and-char system to mitigate climate change and environmental pollution.

Agriculture-based climate change mitigation may occur through enhancing the carbon sink or through reducing greenhouse gases (GHGs) emissions from agricultural residue treatment, as open burning of agricultural residues produces millions of tons of GHGs and air pollutants annually worldwide. Charring slashed biomass, termed as slash-and-char, has been considered as a promising alternative to open burning in dealing with agricultural residues such as rice straw. Previous studies, however, focused on relatively sophisticated slash-and-char systems, which could not be practiced easily by smallholder farmers in developing countries. Here we introduce a simple slash-and-char system to mitigate the environmental problems associated with open burning of rice straw. This system could convert 30.7% of the initial carbon in rice straw into biochar, much higher than that retained in the ash generated by open burning (3.95%). It could also cut GHGs, particulate matters and polycyclic aromatic hydrocarbons (PAHs) emissions by 26.9%, 99.0% and 99.4%, respectively. If open burning of rice straw was replaced by the slash-and-char, the annual emissions of GHGs, particulate matters and PAHs in China would decrease by at least 15.4 Tg, 1.51 Tg and 1.27 Gg, correspondingly. This decrease is nearly twice the size of China's estimated forest C sink (8.81 Tg).