Microbial viruses can control host abundances via density-dependent lytic predator-prey dynamics. Less clear is how temperate viruses, which coexist and replicate with their host, influence microbial communities. Here we show that virus-like particles are relatively less abundant at high host densities. This suggests suppressed lysis where established models predict lytic dynamics are favoured. Meta-analysis of published viral and microbial densities showed that this trend was widespread in diverse ecosystems ranging from soil to freshwater to human lungs. Experimental manipulations showed viral densities more consistent with temperate than lytic life cycles at increasing microbial abundance. An analysis of 24 coral reef viromes showed a relative increase in the abundance of hallmark genes encoded by temperate viruses with increased microbial abundance. Based on these four lines of evidence, we propose the Piggyback-the-Winner model wherein temperate dynamics become increasingly important in ecosystems with high microbial densities; thus 'more microbes, fewer viruses'.
Coral and algal holobionts are assemblages of macroorganisms and microorganisms, including viruses, Bacteria, Archaea, protists and fungi. Despite a decade of research, it remains unclear whether these associations are spatial–temporally stable or species-specific. We hypothesized that conflicting interpretations of the data arise from high noise associated with sporadic microbial symbionts overwhelming signatures of stable holobiont members. To test this hypothesis, the bacterial communities associated with three coral species (Acropora rosaria, Acropora hyacinthus and Porites lutea) and two algal guilds (crustose coralline algae and turf algae) from 131 samples were analyzed using a novel statistical approach termed the Abundance-Ubiquity (AU) test. The AU test determines whether a given bacterial species would be present given additional sampling effort (that is, stable) versus those species that are sporadically associated with a sample. Using the AU test, we show that coral and algal holobionts have a high-diversity group of stable symbionts. Stable symbionts are not exclusive to one species of coral or algae. No single bacterial species was ubiquitously associated with one host, showing that there is not strict heredity of the microbiome. In addition to the stable symbionts, there was a low-diversity community of sporadic symbionts whose abundance varied widely across individual holobionts of the same species. Identification of these two symbiont communities supports the holobiont model and calls into question the hologenome theory of evolution.
Cryophilic algae thrive in liquid water within snow and ice in alpine and polar regions worldwide. Blooms of these algae lower albedo (reflection of sunlight), thereby altering melting patterns (Kohshima, Seko & Yoshimura, 1993; Lutz et al., 2014; Thomas & Duval, 1995). Here metagenomic DNA analysis and satellite imaging were used to investigate red snow in Franz Josef Land in the Russian Arctic. Franz Josef Land red snow metagenomes confirmed that the communities are composed of the autotroph Chlamydomonas nivalis that is supporting a complex viral and heterotrophic bacterial community. Comparisons with white snow communities from other sites suggest that white snow and ice are initially colonized by fungal-dominated communities and then succeeded by the more complex C. nivalis-heterotroph red snow. Satellite image analysis showed that red snow covers up to 80% of the surface of snow and ice fields in Franz Josef Land and globally. Together these results show that C. nivalis supports a local food web that is on the rise as temperatures warm, with potential widespread impacts on alpine and polar environments worldwide.
The majority of microbial communities consist of hundreds to thousands of species, creating a massive network of organisms competing for available resources within an ecosystem. In natural microbial communities, it appears that many microbial species have highly redundant metabolisms and seemingly are capable of utilizing the same substrates. This is paradoxical, as theory indicates that species requiring a common resource should outcompete one another. To better understand why microbial species can coexist, we developed metabolic overlap (MO) as a new metric to survey the functional redundancy of microbial communities at the genome scale across a wide variety of ecosystems. Using metagenome-assembled genomes, we surveyed nearly 1,000 studies across nine ecosystem types. We found the highest MO in extreme (i.e., low pH/high temperature) and aquatic environments, while the lowest MO was observed in communities associated with animal hosts, the built/engineered environment, and soil. In addition, different metabolism subcategories were explored for their degree of MO. For instance, overlap in nitrogen metabolism was among the lowest in animal and engineered ecosystems, while species from the built environment had the highest overlap. Together, we present a metric that utilizes whole genome information to explore overlapping niches of microbes. This provides a detailed picture of potential metabolic competition and cooperation between species present in an ecosystem, indicates the main substrate types sustaining the community, and serves as a valuable tool to generate hypotheses for future research.
Wetland ecosystems are important reservoirs of biodiversity and significantly contribute to emissions of the greenhouse gases CO 2 , N 2 O, and CH 4 . High anthropogenic nitrogen (N) inputs from agriculture and fossil fuel combustion have been recognized as a severe threat to biodiversity and ecosystem functioning, such as control of greenhouse gas emissions. Therefore, it is important to understand how increased N input into pristine wetlands affects the composition and activity of microorganisms, especially in interaction with dominant wetland plants. In a series of incubations analyzed over 90 days, we disentangled the effects of N fertilization on the microbial community in bulk soil and the rhizosphere of Juncus acutiflorus, a common and abundant graminoid wetland plant. We observed an increase in greenhouse gas emissions when N is increased in incubations with J. acutiflorus, changing the system from a greenhouse gas sink to a source. Using 16S rRNA gene amplicon sequencing, we determined that the bacterial orders Opitutales, subgroup 6 Acidobacteria, and Sphingobacteriales significantly responded to high N availability. Based on metagenomic data, we hypothesize that these groups are contributing to the increased greenhouse gas emissions. These results indicated that increased N input leads to shifts in microbial activity within the rhizosphere, altering N cycling dynamics. Our study provides a framework for connecting environmental conditions of wetland bulk and rhizosphere soil to the structure and metabolic output of microbial communities.IMPORTANCE Microorganisms living within the rhizospheres of wetland plants significantly contribute to greenhouse gas emissions. Understanding how microbes produce these gases under conditions that have been imposed by human activities (i.e., nitrogen pollution) is important to the development of future management strategies. Our results illustrate that within the rhizosphere of the wetland plant Juncus acutiflorus, physiological differences associated with nitrogen availability can influence microbial activity linked to greenhouse gas production. By pairing taxonomic information and environmental conditions like nitrogen availability with functional outputs of a system such as greenhouse gas fluxes, we present a framework to link certain taxa to both nitrogen load and greenhouse gas production. We view this type of combined information as essential in moving forward in our understanding of complex systems such as rhizosphere microbial communities.
Wetland ecosystems are important reservoirs of biodiversity and significantly contribute to emissions of the greenhouse gases CO2, N2O and CH4. High anthropogenic nitrogen (N) inputs from agriculture and fossil fuel combustion have been recognized as a severe threat to biodiversity and ecosystem functioning such as control of greenhouse gas emissions. Therefore it is important to understand how increased N input into pristine wetlands affects the composition and activity of micro-organisms, especially in interaction with dominant wetland plants. In a series of incubations analyzed over 90 days, we disentangle the effects of N fertilization on the microbial community in bulk soil and the rhizosphere of Juncus acutiflorus, a common and abundant graminoid wetland plant. We observed an increase in greenhouse gas emissions when N is increased in incubations with J. acutiflorus, changing the system from a greenhouse gas sink to a source. Using 16S rRNA amplicon sequencing and metagenomics, we determined that the bacterial orders Opitutales, Subgroup-6 Acidobacteria and Sphingobacteriales significantly responded to high N availability and we hypothesize that these groups are contributing to the increased greenhouse gas emissions. These results indicated that increased N input leads to shifts in microbial activity within the rhizosphere, severely altering N cycling dynamics. Our study provides a framework for connecting environmental conditions of wetland bulk and rhizosphere soil to the structure and metabolic output of microbial communities.
Anaerobic ammonium-oxidizing (anammox) bacteria convert nitrite and ammonium via nitric oxide (NO) and hydrazine into dinitrogen gas by using a diverse array of proteins, including numerous c-type cytochromes. Many new catalytic and spectroscopic properties of ctype cytochromes have been unraveled by studies on the biochemical pathways underlying the anammox process. The unique anammox intermediate hydrazine is produced by a multiheme cytochrome c protein, hydrazine synthase, through the comproportionation of ammonium and NO and the input of three electrons. It is unclear how these electrons are delivered to hydrazine synthase. Here, we report the discovery of a functional tetraheme c-type cytochrome from the anammox bacterium Kuenenia stuttgartiensis with a naturally occurring contracted Cys-Lys-Cys-His (CKCH) heme-binding motif, which is encoded in the hydrazine synthase gene cluster. The purified tetraheme protein (named here KsTH) exchanged electrons with hydrazine synthase. Complementary spectroscopic techniques revealed that this protein harbors four low-spin hexacoordinated hemes with His/Lys (heme 1), His/Cys (heme 2), and two His/His ligations (hemes 3 and 4). A genomic database search revealed that c-type cytochromes with a contracted CXCH heme-binding motif are present throughout the bacterial and archaeal domains in the tree of life, suggesting that this heme recognition site may be employed by many different groups of microorganisms.
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