A single genus in the gut microbiome reflects host preference and specificity

Eren, A. Murat; Sogin, Mitchell L.; Morrison, Hilary G.; Vineis, Joseph H.; Fisher, James S.; Newton, Ryan J.; McLellan, Sandra L.

doi:10.1038/ismej.2014.97

Cited by 149 publications

(140 citation statements)

References 54 publications

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“…The filters were stored in cryovials at Ϫ80°C until the DNA extraction procedure. We previously sequenced DNA extracted from 53 fecal samples from animals (cats, chickens, cows, deer, dogs, swine) and two primary influent sewage samples and reported on the fine-scale population structure within the genus Blautia (35). The environmental samples and additional sewage samples analyzed in this study were also sequenced previously, and methods for their collection and processing are reported elsewhere (18,36).…”

Section: Methodsmentioning

confidence: 99%

Comparison of Sewage and Animal Fecal Microbiomes by Using Oligotyping Reveals Potential Human Fecal Indicators in Multiple Taxonomic Groups

Fisher

Eren

Green

et al. 2015

Appl Environ Microbiol

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dMost DNA-based microbial source tracking (MST) approaches target host-associated organisms within the order Bacteroidales, but the gut microbiota of humans and other animals contain organisms from an array of other taxonomic groups that might provide indicators of fecal pollution sources. To discern between human and nonhuman fecal sources, we compared the V6 regions of the 16S rRNA genes detected in fecal samples from six animal hosts to those found in sewage (as a proxy for humans). We focused on 10 abundant genera and used oligotyping, which can detect subtle differences between rRNA gene sequences from ecologically distinct organisms. Our analysis showed clear patterns of differential oligotype distributions between sewage and animal samples. Over 100 oligotypes of human origin occurred preferentially in sewage samples, and 99 human oligotypes were sewage specific. Sequences represented by the sewage-specific oligotypes can be used individually for development of PCRbased assays or together with the oligotypes preferentially associated with sewage to implement a signature-based approach. Analysis of sewage from Spain and Brazil showed that the sewage-specific oligotypes identified in U.S. sewage have the potential to be used as global alternative indicators of human fecal pollution. Environmental samples with evidence of prior human fecal contamination had consistent ratios of sewage signature oligotypes that corresponded to the trends observed for sewage. Our methodology represents a promising approach to identifying new bacterial taxa for MST applications and further highlights the potential of the family Lachnospiraceae to provide human-specific markers. In addition to source tracking applications, the patterns of the fine-scale population structure within fecal taxa suggest a fundamental relationship between bacteria and their hosts. Microbial source tracking (MST) is used to determine sources of fecal pollution in surface waters and recreational beaches with the goal of minimizing the risk to human health (1-3). Transmission of bacterial, viral, and zoonotic diseases occurs through feces-contaminated water (4), and identification of the type of host inputs (e.g., sewage, wildlife, agricultural) can provide a more accurate assessment of the risks to human health and better direct management actions to reduce likely sources of pollution (5). Identification of fecal sources is based on the assumption that some microorganisms exhibit host-specific distribution patterns (6). The majority of microbial population studies performed to identify members that specifically or preferentially associate with particular animal hosts have used the 16S rRNA gene as a marker (7-9).Bacteria within the order Bacteroidales have been the major focus of molecular MST efforts (10-16), as they have many qualities that make them an effective indicator. These organisms are abundant in the gastrointestinal tract of many animals, some species exhibit an association with particular hosts, and many have persistence and survival chara...

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Section: Methodsmentioning

confidence: 99%

Comparison of Sewage and Animal Fecal Microbiomes by Using Oligotyping Reveals Potential Human Fecal Indicators in Multiple Taxonomic Groups

Fisher

Eren

Green

et al. 2015

Appl Environ Microbiol

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“…This method has been previously used for numerous applications. For example, oligotyping has been used to identify host specificity of Blautia, to explore the ecology of Arcobacter in sewage, and to reveal habitat preferences of Vibrio (31)(32)(33). To assess the levels of E. coli and enterococcus reads in our community sequences, we used the SRA BLAST tool.…”

Section: Methodsmentioning

confidence: 99%

Influence of Land Use, Nutrients, and Geography on Microbial Communities and Fecal Indicator Abundance at Lake Michigan Beaches

Cloutier

Alm

McLellan

2015

Appl Environ Microbiol

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bMicrobial communities within beach sand play a key role in nutrient cycling and are important to the nearshore ecosystem function. Escherichia coli and enterococci, two common indicators of fecal pollution, have been shown to persist in the beach sand, but little is known about how microbial community assemblages are related to these fecal indicator bacteria (FIB) reservoirs. We examined eight beaches across a geographic gradient and range of land use types and characterized the indigenous community structure in the water and the backshore, berm, and submerged sands. FIB were found at similar levels in sand at beaches adjacent to urban, forested, and agricultural land and in both the berm and backshore. However, there were striking differences in the berm and backshore microbial communities, even within the same beach, reflecting the very different environmental conditions in these beach zones in which FIB can survive. In contrast, the microbial communities in a particular beach zone were similar among beaches, including at beaches on opposite shores of Lake Michigan. The differences in the microbial communities that did exist within a beach zone correlated to nutrient levels, which varied among geographic locations. Total organic carbon and total phosphorus were higher in Wisconsin beach sand than in beach sand from Michigan. Within predominate genera, finescale sequence differences could be found that distinguished the populations from the two states, suggesting a biogeographic effect. This work demonstrates that microbial communities are reflective of environmental conditions at freshwater beaches and are able to provide useful information regarding long-term anthropogenic stress. Since the creation of the Federal Beach Environmental Assessment and Coastal Health (BEACH) Act of 2000, coastal communities have been challenged with implementing programs for the monitoring of recreational waters. Water quality monitoring relies on fecal indicator bacteria (FIB), such as Escherichia coli and enterococci, and the assumption that both are fecal in origin. In recent years, many Great Lakes coastal recreational waters were monitored for the first time and subsequently were found to have unacceptable levels of E. coli, indicating the presence of contamination from sources such as sewage, stormwater, or agricultural runoff. However, recent studies have detected high concentrations of FIB in recreational beach sands compared to the concentrations in the nearby monitored waters (1-4). Importantly, several studies have documented that sand reservoirs of FIB play a large role in beach water samples exceeding regulatory limits (1, 3, 5-7).Persistent FIB in the beach environment is of great concern. The presence of FIB in either recreational waters or sand is assumed to indicate a recent pollution event. However, the persistence and possible proliferation of FIB in the beach environment can confound beach-monitoring efforts and poses additional challenges for beach managers. In addition, there is mounting evidence that E. co...

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“…Mounting evidence suggests that many gut microbes are host-specific, [54][55][56] preferentially associating with a particular species over any other potential host or environment. Thus far, however, correlational data is in much greater abundance than elucidated causal mechanisms.…”

Section: Conclusion and Perspectivementioning

confidence: 99%