DISTINCT INTESTINAL MICROBIAL COMMUNITIES OF TWO SYMPATRIC ANADROMOUS ARCTIC SALMONIDS AND THE EFFECTS OF MIGRATION AND FEEDING

Although intestinal microbial communities from anadromous Arctic char (Salvelinus alpinus) in Kitikmeot, Nunavut, differ depending on the timing and location of capture, determinants of gut microbiota in other wild Arctic salmonids are largely unknown. Using high-throughput 16S rRNA gene sequence data, we compared intestinal microbiota from Arctic char to those from a related and sympatric salmonid, lake whitefish (Coregonus clupeaformis). Shifts in lake whitefish gut microbial community composition were observed between brackish and freshwaters, similar to impacts of salinity reported previously for Arctic char. Despite these similarities, gut community profiles for the two salmonids differed, whitefish having higher diversities and increased proportions of taxa affiliated with potential pathogens. Geography seemed to have a greater impact on freshwater whitefish gut microbiota than on corresponding Arctic char. Additionally, microbiota diversity was significantly more affected by feeding behavior in whitefish compared to sympatric Arctic char. Since sampled whitefish were at their northern range limits and grew slowly, we speculate that they, and their microbial consortia, could be more vulnerable to certain abiotic and biotic factors than Arctic char, which are well adapted to conditions found in these high latitude environments and have the most northerly distribution of any freshwater fish.

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Fluoxetine-induced alteration of murine gut microbial community structure: evidence for a microbial endocrinology-based mechanism of action responsible for fluoxetine-induced side effects

PeerJ ◽

10.7717/peerj.6199 ◽

2019 ◽

Vol 7 ◽

pp. e6199 ◽

Cited By ~ 16

Author(s):

Mark Lyte ◽

Karrie M. Daniels ◽

Stephan Schmitz-Esser

Keyword(s):

Body Weight ◽

Weight Gain ◽

Side Effects ◽

Gut Microbiota ◽

Microbial Communities ◽

Time Course ◽

Selective Serotonin Reuptake Inhibitors ◽

Sequence Data ◽

Rrna Gene ◽

Dosing Regimen

Background Depression and major depressive disorder affect 25% of the population. First line treatment utilizing selective serotonin reuptake inhibitors (SSRIs) have met with limited success due to well-recognized negative side effects which include weight gain or loss. This inability to control unwanted side effects often result in patients stopping their antidepressant medications. The mechanisms underlying the failure of SSRIs are incompletely understood. Methods Male CF-1 mice (5 weeks of age, N = 10 per group) were per orally administered fluoxetine (20 mg per kg body weight) or diluent daily for 29 days. During this time fecal specimens were collected at three defined time points (0, 15 and 29 days). At the conclusion of the 29-day dosing regimen, animals were subjected to two behavioral assessments. For bacterial identification of the microbiota, 16S rRNA gene sequencing was performed on 60 fecal specimens (three specimens per mouse time course, N = 20 mice) using Illumina MiSeq. Analysis of community sequence data was done using mothur and LEfSe bioinformatic software packages. Results Daily per oral administration of fluoxetine for 29 days to male mice resulted in a significant, time dependent, alteration in microbial communities accompanying changes in body weight. The calculated species richness and diversity indicators of the murine fecal microbial communities were inconsistent and not significantly different between the groups. Among the phylotypes decreased in abundance due to fluoxetine administration were Lactobacillus johnsonii and Bacteroidales S24-7 which belong to phyla associated with regulation of body mass. The observed changes in body weight due to fluoxetine administration mimicked the dramatic shifts in weight gain/loss that has been observed in humans. Further, at the conclusion of the 29-day dosing regimen fluoxetine-dosed animals evidenced a mild anxiogenic-like behavior. Discussion We report that the most widely used antidepressant, fluoxetine, which is an SSRI-type drug, results in the selective depletion of gut microbiota, specifically the Lactobacilli which are involved in the regulation of body weight. Concomitantly, fluoxetine administration increases the abundance of phylotypes related to dysbiosis. Since Lactobacilli have been previously shown to possess a known biogenic amine transporter that regulates the uptake of fluoxetine, it is proposed that a microbial endocrinology-based mechanistic pathway is responsible for the ability of SSRIs to selectively negatively impact beneficial microbiota. The results of this study therefore suggest that the negative clinical side effects due to fluoxetine administration may be due to alterations in gut microbiota. Further, the data also suggests that supplementation of bacterial genera directly affected by fluoxetine administration may prove useful in ameliorating some of the well-known side effects of chronic fluoxetine administration such as weight alterations.

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Comparative Analysis of the Gut Microbiota of Adult Mosquitoes From Eight Locations in Hainan, China

Frontiers in Cellular and Infection Microbiology ◽

10.3389/fcimb.2020.596750 ◽

2020 ◽

Vol 10 ◽

Author(s):

Xun Kang ◽

Yanhong Wang ◽

Siping Li ◽

Xiaomei Sun ◽

Xiangyang Lu ◽

...

Keyword(s):

Gut Microbiota ◽

Disease Control ◽

Bacterial Communities ◽

Mosquito Species ◽

Microbial Community Composition ◽

Variable Region ◽

Rrna Gene ◽

Microbial Composition ◽

Quality Filtering ◽

And Function

The midgut microbial community composition, structure, and function of field-collected mosquitoes may provide a way to exploit microbial function for mosquito-borne disease control. However, it is unclear how adult mosquitoes acquire their microbiome, how the microbiome affects life history traits and how the microbiome influences community structure. We analyzed the composition of 501 midgut bacterial communities from field-collected adult female mosquitoes, including Aedes albopictus, Aedes galloisi, Culex pallidothorax, Culex pipiens, Culex gelidus, and Armigeres subalbatus, across eight habitats using the HiSeq 4000 system and the V3−V4 hyper-variable region of 16S rRNA gene. After quality filtering and rarefaction, a total of 1421 operational taxonomic units, belonging to 29 phyla, 44 families, and 43 genera were identified. Proteobacteria (75.67%) were the most common phylum, followed by Firmicutes (10.38%), Bacteroidetes (6.87%), Thermi (4.60%), and Actinobacteria (1.58%). The genera Rickettsiaceae (33.00%), Enterobacteriaceae (20.27%), Enterococcaceae (7.49%), Aeromonadaceae (7.00%), Thermaceae (4.52%), and Moraxellaceae (4.31%) were dominant in the samples analyzed and accounted for 76.59% of the total genera. We characterized the midgut bacterial communities of six mosquito species in Hainan province, China. The gut bacterial communities were different in composition and abundance, among locations, for all mosquito species. There were significant differences in the gut microbial composition between some species and substantial variation in the gut microbiota between individuals of the same mosquito species. There was a marked variation in different mosquito gut microbiota within the same location. These results might be useful in the identification of microbial communities that could be exploited for disease control.

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Ontogenetic Differences in Dietary Fat Influence Microbiota Assembly in the Zebrafish Gut

mBio ◽

10.1128/mbio.00687-15 ◽

2015 ◽

Vol 6 (5) ◽

Cited By ~ 50

Author(s):

Sandi Wong ◽

W. Zac Stephens ◽

Adam R. Burns ◽

Keaton Stagaman ◽

Lawrence A. David ◽

...

Keyword(s):

Gut Microbiota ◽

Microbial Communities ◽

Dietary Fat ◽

Rrna Gene ◽

Microbiota Composition ◽

Ideal Model ◽

Surrounding Environment ◽

Animal Hosts ◽

The Relationship ◽

Gut Microbiota Composition

ABSTRACT Gut microbiota influence the development and physiology of their animal hosts, and these effects are determined in part by the composition of these microbial communities. Gut microbiota composition can be affected by introduction of microbes from the environment, changes in the gut habitat during development, and acute dietary alterations. However, little is known about the relationship between gut and environmental microbiotas or about how host development and dietary differences during development impact the assembly of gut microbiota. We sought to explore these relationships using zebrafish, an ideal model because they are constantly immersed in a defined environment and can be fed the same diet for their entire lives. We conducted a cross-sectional study in zebrafish raised on a high-fat, control, or low-fat diet and used bacterial 16S rRNA gene sequencing to survey microbial communities in the gut and external environment at different developmental ages. Gut and environmental microbiota compositions rapidly diverged following the initiation of feeding and became increasingly different as zebrafish grew under conditions of a constant diet. Different dietary fat levels were associated with distinct gut microbiota compositions at different ages. In addition to alterations in individual bacterial taxa, we identified putative assemblages of bacterial lineages that covaried in abundance as a function of age, diet, and location. These results reveal dynamic relationships between dietary fat levels and the microbial communities residing in the intestine and the surrounding environment during ontogenesis. IMPORTANCE The ability of gut microbiota to influence host health is determined in part by their composition. However, little is known about the relationship between gut and environmental microbiotas or about how ontogenetic differences in dietary fat impact gut microbiota composition. We addressed these gaps in knowledge using zebrafish, an ideal model organism because their environment can be thoroughly sampled and they can be fed the same diet for their entire lives. We found that microbial communities in the gut changed as zebrafish aged under conditions of a constant diet and became increasingly different from microbial communities in their surrounding environment. Further, we observed that the amount of fat in the diet had distinct age-specific effects on gut community assembly. These results reveal the complex relationships between microbial communities residing in the intestine and those in the surrounding environment and show that these relationships are shaped by dietary fat throughout the life of animal hosts.

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Changes in the Active, Dead, and Dormant Microbial Community Structure across a Pleistocene Permafrost Chronosequence

Applied and Environmental Microbiology ◽

10.1128/aem.02646-18 ◽

2019 ◽

Vol 85 (7) ◽

Cited By ~ 17

Author(s):

Alexander Burkert ◽

Thomas A. Douglas ◽

Mark P. Waldrop ◽

Rachel Mackelprang

Keyword(s):

Microbial Community ◽

16S Rrna ◽

16S Rrna Gene ◽

Microbial Communities ◽

Community Composition ◽

Environmental Conditions ◽

Microbial Community Composition ◽

Rrna Gene ◽

Subzero Temperatures ◽

Dormant Cells

ABSTRACTPermafrost hosts a community of microorganisms that survive and reproduce for millennia despite extreme environmental conditions, such as water stress, subzero temperatures, high salinity, and low nutrient availability. Many studies focused on permafrost microbial community composition use DNA-based methods, such as metagenomics and 16S rRNA gene sequencing. However, these methods do not distinguish among active, dead, and dormant cells. This is of particular concern in ancient permafrost, where constant subzero temperatures preserve DNA from dead organisms and dormancy may be a common survival strategy. To circumvent this, we applied (i) LIVE/DEAD differential staining coupled with microscopy, (ii) endospore enrichment, and (iii) selective depletion of DNA from dead cells to permafrost microbial communities across a Pleistocene permafrost chronosequence (19,000, 27,000, and 33,000 years old). Cell counts and analysis of 16S rRNA gene amplicons from live, dead, and dormant cells revealed how communities differ between these pools, how they are influenced by soil physicochemical properties, and whether they change over geologic time. We found evidence that cells capable of forming endospores are not necessarily dormant and that members of the classBacilliwere more likely to form endospores in response to long-term stressors associated with permafrost environmental conditions than members of theClostridia, which were more likely to persist as vegetative cells in our older samples. We also found that removing exogenous “relic” DNA preserved within permafrost did not significantly alter microbial community composition. These results link the live, dead, and dormant microbial communities to physicochemical characteristics and provide insights into the survival of microbial communities in ancient permafrost.IMPORTANCEPermafrost soils store more than half of Earth’s soil carbon despite covering ∼15% of the land area (C. Tarnocai et al., Global Biogeochem Cycles 23:GB2023, 2009, https://doi.org/10.1029/2008GB003327). This permafrost carbon is rapidly degraded following a thaw (E. A. G. Schuur et al., Nature 520:171–179, 2015, https://doi.org/10.1038/nature14338). Understanding microbial communities in permafrost will contribute to the knowledge base necessary to understand the rates and forms of permafrost C and N cycling postthaw. Permafrost is also an analog for frozen extraterrestrial environments, and evidence of viable organisms in ancient permafrost is of interest to those searching for potential life on distant worlds. If we can identify strategies microbial communities utilize to survive in permafrost, it may yield insights into how life (if it exists) survives in frozen environments outside of Earth. Our work is significant because it contributes to an understanding of how microbial life adapts and survives in the extreme environmental conditions in permafrost terrains.

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Assessment of Microbial Communities by Graph Partitioning in a Study of Soil Fungi in Two Alpine Meadows

Applied and Environmental Microbiology ◽

10.1128/aem.00748-09 ◽

2009 ◽

Vol 75 (18) ◽

pp. 5863-5870 ◽

Cited By ~ 17

Author(s):

L. Zinger ◽

E. Coissac ◽

P. Choler ◽

R. A. Geremia

Keyword(s):

Microbial Communities ◽

Graph Partitioning ◽

Sequence Data ◽

Large Subunit ◽

Fungal Communities ◽

Rrna Gene ◽

Data Sets ◽

Alignment Algorithm ◽

Single Linkage ◽

Phylogenetic Structure

ABSTRACT Understanding how microbial community structure and diversity respond to environmental conditions is one of the main challenges in environmental microbiology. However, there is often confusion between determining the phylogenetic structure of microbial communities and assessing the distribution and diversity of molecular operational taxonomic units (MOTUs) in these communities. This has led to the use of sequence analysis tools such as multiple alignments and hierarchical clustering that are not adapted to the analysis of large and diverse data sets and not always justified for characterization of MOTUs. Here, we developed an approach combining a pairwise alignment algorithm and graph partitioning by using MCL (Markov clustering) in order to generate discrete groups for nuclear large-subunit rRNA gene and internal transcript spacer 1 sequence data sets obtained from a yearly monitoring study of two spatially close but ecologically contrasting alpine soils (namely, early and late snowmelt locations). We compared MCL with a classical single-linkage method (Ccomps) and showed that MCL reduced bias such as the chaining effect. Using MCL, we characterized fungal communities in early and late snowmelt locations. We found contrasting distributions of MOTUs in the two soils, suggesting that there is a high level of habitat filtering in the assembly of alpine soil fungal communities. However, few MOTUs were specific to one location.

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Parallel and non-parallel changes of the gut microbiota during trophic diversification in repeated young adaptive radiations of sympatric cichlid fish

10.21203/rs.3.rs-20414/v3 ◽

2020 ◽

Author(s):

Andreas Härer ◽

Julián Torres-Dowdall ◽

Sina J. Rometsch ◽

Elizabeth Yohannes ◽

Gonzalo Machado-Schiaffino ◽

...

Keyword(s):

Gut Microbiota ◽

Microbial Communities ◽

Trophic Ecology ◽

Cichlid Fish ◽

Conclusive Evidence ◽

Rrna Gene ◽

Crater Lakes ◽

Ecological Diversification ◽

Early Stages ◽

Adaptive Radiations

Abstract Background: Recent increases in understanding the ecological and evolutionary roles of microbial communities has underscored the importance for their hosts’ biology. Yet, little is known about gut microbiota dynamics during early stages of ecological diversification and speciation. We sequenced the V4 region of the 16s rRNA gene to study the gut microbiota of Nicaraguan Midas cichlid fish (Amphilophus cf. citrinellus). Specifically, we tested the hypothesis that parallel divergence in trophic ecology in extremely young adaptive radiations from two crater lakes is associated with parallel changes of their gut microbiota. Results: Bacterial communities of fish guts and lake water were highly distinct, indicating that the gut microbiota is shaped by host-specific factors. Among individuals of the same crater lake, differentiation in trophic ecology was weakly associated with gut microbiota differentiation, suggesting that diet, to some extent, affects the gut microbiota. However, differences in trophic ecology were much more pronounced across than within species whereas similar patterns were not observed for taxonomic and functional differences of the gut microbiota. Across the two crater lakes, we could not detect conclusive evidence for parallel changes of the gut microbiota associated with trophic ecology. Conclusions: A lack of clearly differentiated niches during early stages of ecological diversification might result in non-parallel changes of gut microbial communities, as observed in our study system as well as in other recently diverged fish species.

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Community composition and development of the post-weaning piglet gut microbiome

10.21203/rs.3.rs-60981/v1 ◽

2020 ◽

Author(s):

Daniela Gaio ◽

Matthew Z DeMaere ◽

Kay Anantanawat ◽

Graeme J Eamens ◽

Michael Liu ◽

...

Keyword(s):

Microbial Community ◽

Gut Microbiota ◽

Community Composition ◽

Antibiotic Treatment ◽

Gut Microbiome ◽

Treatment Effects ◽

Sequence Data ◽

Microbial Community Composition ◽

Dominant Factor ◽

Microbial Composition

Abstract BackgroundEarly weaning and intensive farming practices predispose piglets to the development of infectious and often lethal diseases, against which antibiotics are used. Besides contributing to the build-up of antimicrobial resistance, antibiotics are known to modulate the gut microbial composition. Studies have previously investigated the effects of probiotics as alternatives to antibiotic treatment for the prevention of post-weaning diarrhea. In order to describe the post-weaning gut microbiota, and the effects of two probiotics formulations and of intramuscular antibiotic treatment on the gut microbiota, we processed over 800 faecal time-series samples from 126 piglets and 42 sows, generating over 8Tbp of metagenomic shotgun sequence data. Here we describe the animal trial procedures, the generation of our metagenomic dataset and the analysis of the microbial community composition using a phylogenetic framework.ResultsFactors such as age, litter effects, and breed, by significantly correlating with gut microbial community shifts, can be major confounding factors in the assessment of treatment effects. Intramuscular antibiotic treatment and probiotic treatments were found to correlate with alpha and beta diversity, as well as with a transient establishment of Mollicutes and Lactobacillales, respectively. We found the abundance of certain taxa to correlate with weight gain.ConclusionsOur findings demonstrate that breed, litter, and age, are important contributors to variation in the community composition, and that treatment effects of the antibiotic and probiotic treatments were subtle, while host age was the dominant factor in shaping the gut microbiota of piglets after weaning. The current study shows, by means of a phylogenetic diversity framework, that the post-weaning pig gut microbiome appears to follow a highly structured developmental program with characteristic post-weaning changes that can distinguish hosts that were born as little as two days apart in the second month of life.

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Parallel and non-parallel changes of the gut microbiota during trophic diversification in repeated young adaptive radiations of sympatric cichlid fish

10.21203/rs.3.rs-20414/v1 ◽

2020 ◽

Author(s):

Andreas Härer ◽

Julián Torres-Dowdall ◽

Sina J. Rometsch ◽

Elizabeth Yohannes ◽

Gonzalo Machado-Schiaffino ◽

...

Keyword(s):

Gut Microbiota ◽

Microbial Communities ◽

Trophic Ecology ◽

Cichlid Fish ◽

Conclusive Evidence ◽

Rrna Gene ◽

Crater Lakes ◽

Ecological Diversification ◽

Early Stages ◽

Adaptive Radiations

Abstract Background: Recent increases in understanding the ecological and evolutionary roles of microbial communities has underscored the importance for their hosts’ biology. Yet, little is known about gut microbiota dynamics during early stages of ecological diversification and speciation. We sequenced the V4 region of the 16s rRNA gene to study the gut microbiota of Nicaraguan Midas cichlid fish ( Amphilophus cf. citrinellus ). Specifically, we tested the hypothesis that parallel divergence in trophic ecology in extremely young adaptive radiations from two crater lakes is associated with parallel changes of their gut microbiota.Results: Bacterial communities of fish guts and lake water were highly distinct, indicating that the gut microbiota is shaped by host-specific factors. Among individuals of the same crater lake, differentiation in trophic ecology was weakly associated with gut microbiota differentiation, suggesting that diet, to some extent, affects the gut microbiota. However, differences in trophic ecology were much more pronounced across than within species whereas similar patterns were not observed for taxonomic and functional differences of the gut microbiota. Across the two crater lakes, we could not detect conclusive evidence for parallel changes of the gut microbiota associated with trophic ecology.Conclusions: A lack of clearly differentiated niches during early stages of ecological diversification might result in non-parallel changes of gut microbial communities, as observed in our study system as well as in other recently diverged fish species.

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Disentangling the Relative Roles of Vertical Transmission, Subsequent Colonizations, and Diet on Cockroach Microbiome Assembly

mSphere ◽

10.1128/msphere.01023-20 ◽

2021 ◽

Vol 6 (1) ◽

Author(s):

Justinn Renelies-Hamilton ◽

Kristjan Germer ◽

David Sillam-Dussès ◽

Kasun H. Bodawatta ◽

Michael Poulsen

Keyword(s):

Gut Microbiota ◽

Microbial Communities ◽

Vertical Transmission ◽

Priority Effects ◽

Rrna Gene ◽

Combined Effects ◽

Microbial Composition ◽

Host Fitness ◽

Microbial Invasion ◽

Host Taxon

ABSTRACT A multitude of factors affect the assemblies of complex microbial communities associated with animal hosts, with implications for community flexibility, resilience, and long-term stability; however, their relative effects have rarely been deduced. Here, we use a tractable lab model to quantify the relative and combined effects of parental transmission (egg case microbiome present/reduced), gut inocula (cockroach versus termite gut provisioned), and varying diets (matched or unmatched with gut inoculum source) on gut microbiota structure of hatchlings of the omnivorous cockroach Shelfordella lateralis using 16S rRNA gene (rDNA) amplicon sequencing. We show that the presence of a preexisting bacterial community via vertical transmission of microbes on egg cases reduces subsequent microbial invasion, suggesting priority effects that allow initial colonizers to take a strong hold and which stabilize the microbiome. However, subsequent inoculation sources more strongly affect ultimate community composition and their ecological networks, with distinct host-taxon-of-origin effects on which bacteria establish. While this is so, communities respond flexibly to specific diets in ways that consequently impact predicted community functions. In conclusion, our findings suggest that inoculations drive communities toward different stable states depending on colonization and extinction events, through ecological host-microbe relations and interactions with other gut bacteria, while diet in parallel shapes the functional capabilities of these microbiomes. These effects may lead to consistent microbial communities that maximize the extended phenotype that the microbiota provides the host, particularly if microbes spend most of their lives in host-associated environments. IMPORTANCE When host fitness is dependent on gut microbiota, microbial community flexibility and reproducibility enhance host fitness by allowing fine-tuned environmental tracking and sufficient stability for host traits to evolve. Our findings lend support to the importance of vertically transmitted early-life microbiota as stabilizers, through interactions with potential colonizers, which may contribute to ensuring that the microbiota aligns within host fitness-enhancing parameters. Subsequent colonizations are driven by microbial composition of the sources available, and we confirm that host-taxon-of-origin affects stable subsequent communities, while communities at the same time retain sufficient flexibility to shift in response to available diets. Microbiome structure is thus the result of the relative impact and combined effects of inocula and fluctuations driven by environment-specific microbial sources and digestive needs. These affect short-term community structure on an ecological time scale but could ultimately shape host species specificities in microbiomes across evolutionary time, if environmental conditions prevail.

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Ultrahigh-Throughput Multiplexing and Sequencing of >500-Base-Pair Amplicon Regions on the Illumina HiSeq 2500 Platform

mSystems ◽

10.1128/msystems.00029-19 ◽

2019 ◽

Vol 4 (1) ◽

Cited By ~ 17

Author(s):

Johanna B. Holm ◽

Michael S. Humphrys ◽

Courtney K. Robinson ◽

Matthew L. Settles ◽

Sandra Ott ◽

...

Keyword(s):

High Throughput Sequencing ◽

Sequence Data ◽

Microbial Community Composition ◽

Pcr Amplification ◽

Illumina Miseq ◽

Amplicon Sequencing ◽

Rrna Gene ◽

Illumina Hiseq ◽

Illumina Miseq Platform ◽

Miseq Platform

ABSTRACT Amplification, sequencing, and analysis of the 16S rRNA gene affords characterization of microbial community composition. As this tool has become more popular and amplicon-sequencing applications have grown in the total number of samples, growth in sample multiplexing is becoming necessary while maintaining high sequence quality and sequencing depth. Here, modifications to the Illumina HiSeq 2500 platform are described which produce greater multiplexing capabilities and 300-bp paired-end reads of higher quality than those produced by the current Illumina MiSeq platform. To improve the feasibility and flexibility of this method, a 2-step PCR amplification protocol is also described that allows for targeting of different amplicon regions, and enhances amplification success from samples with low bacterial bioburden. IMPORTANCE Amplicon sequencing has become a popular and widespread tool for surveying microbial communities. Lower overall costs associated with high-throughput sequencing have made it a widely adopted approach, especially for projects that necessitate sample multiplexing to eliminate batch effect and reduced time to acquire data. The method for amplicon sequencing on the Illumina HiSeq 2500 platform described here provides improved multiplexing capabilities while simultaneously producing greater quality sequence data and lower per-sample cost relative to those of the Illumina MiSeq platform without sacrificing amplicon length. To make this method more flexible for various amplicon-targeted regions as well as improve amplification from low-biomass samples, we also present and validate a 2-step PCR library preparation method.

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