Mesophilic and thermophilic viruses are associated with nutrient cycling during hyperthermophilic composting

Abstract

While decomposition of organic matter by bacteria plays a major role in nutrient cycling in terrestrial ecosystems, the significance of viruses remains poorly understood. Here we combined metagenomics and metatranscriptomics with temporal sampling to study the significance of mesophilic and thermophilic bacteria and their viruses on nutrient cycling during industrial-scale hyperthermophilic composting (HTC). Our results show that virus-bacteria density dynamics and activity are tightly coupled, where viruses specific to mesophilic and thermophilic bacteria track their host densities, triggering microbial community succession via top-down control during HTC. Moreover, viruses specific to mesophilic bacteria encoded and expressed several auxiliary metabolic genes (AMGs) linked to carbon cycling, impacting nutrient turnover alongside bacteria. Nutrient turnover correlated positively with virus–host ratio, indicative of a positive relationship between ecosystem functioning, viral abundances, and viral activity. These effects were predominantly driven by DNA viruses as most detected RNA viruses were associated with eukaryotes and not associated with nutrient cycling during the thermophilic phase of composting. Our findings suggest that DNA viruses could drive nutrient cycling during HTC by recycling bacterial biomass through cell lysis and by expressing key AMGs. Viruses could hence potentially be used as indicators of microbial ecosystem functioning to optimize productivity of biotechnological and agricultural systems.

Enhanced Bacterium–Phage Symbiosis in Attached Microbial Aggregates on a Membrane Surface Facing Elevated Hydraulic Stress

“…The high lysogenicity of phageome and bacteriome has also been reported in recent investigations of virome in a wastewater treatment plant. 87 Similar to other habitats under elevated environmental stress, phage community tended to exhibit a broad host range 20,43,44 when colonized to the membrane surface facing great hydraulic pressure, along with other environmental stresses. Bacterium−Phage Interactions Differed between Habitats and Seasons.…”

“…18,19 Recent researchers have uncovered the variation of bacterium−phage interactions in response to environmental stress. 20,21 However, it remains largely unexplored how microbial aggregate habitats (and their associated microenvironments) influence bacterium−phage interactions and virome functions. Therefore, it is crucial to illuminate bacterium−phage interactions in microbial aggregates of engineered systems.…”

“…Phages are bacterial viruses that are increasingly recognized for their prevalence and importance in microbial communities . Phages can mediate bacterial mortality and metabolism through lytic and lysogenic infections, which further influence the microbiome structure and functions. , Especially, the biological reactors of wastewater treatment plants harbor highly abundant and diverse phages that closely interact with their bacterial hosts. , Moreover, phages are potentially involved in mediating host metabolism by carrying extensive auxiliary metabolic genes (AMGs) associated with microbial carbon and nutrient cycling in this engineered system. , Recent researchers have uncovered the variation of bacterium–phage interactions in response to environmental stress. , However, it remains largely unexplored how microbial aggregate habitats (and their associated microenvironments) influence bacterium–phage interactions and virome functions. Therefore, it is crucial to illuminate bacterium–phage interactions in microbial aggregates of engineered systems.…”

The role of rhizosphere phages in soil health

“…These external factors can also influence the intrinsic dynamics between phages and their host, e.g. by triggering population fluctuations and ecological succession in microbial communities, which can feed back to ecosystem functioning (Liao et al 2023 , Santos-Medellin et al 2023 ). The emergence of novel methodologies for purifying, extracting, and quantifying phage assemblages from soils (Williamson et al 2003 ), coupled with advancements in metagenomic sequencing, has paved the way for a more in-depth exploration of the true soil phage diversity (Paez-Espino et al 2019 , Koonin and Yutin 2020 , Roux and Emerson 2022 , Mabrouk et al 2023 ), while metatranscriptomic approaches have opened the door to study phage activity and RNA phage diversity (Callanan et al 2020 , Neri et al 2022 ).…”

“…For instance, phages that infect nitrogen-fixing rhizobia bacteria, have been shown to reduce nodulation by phage-sensitive rhizobia, thus influencing nitrogen fixation in legume–rhizobium symbiosis (Evans et al 1979 , Sharma et al 2002 ). Recently, temporal changes in phage communities were linked with nutrient cycling during composting, where phages specific to mesophilic and thermophilic bacteria tracked their host densities, triggering bacteria-phage community succession via top-down control (Liao et al 2023 ). Crucially, nutrient turnover correlated positively with virus–host ratio, indicative of a positive relationship between ecosystem functioning, viral abundances, and viral activity (Liao et al 2023 ).…”