Cartography of opportunistic pathogens and antibiotic resistance genes in a tertiary hospital environment

Chng, Kern Rei; Li, Chenhao; Bertrand, Denis; Ng, Amanda Hui Qi; Kwah, Junmei Samantha; Low, Hwee Meng; Tong, Chengxuan; Natrajan, Maanasa; Zhang, Michael Hongjie; Xu, Licheng; Ko, Karrie Kwan Ki; Ho, Eliza Xin Pei; Av-Shalom, Tamar V.; Teo, Jeanette Woon Pei; Khor, Chiea Chuen; Chen, Swaine L.; Mason, Christopher E.; Ng, Oon Tek; Marimuthu, Kalisvar; Ang, Brenda; Nagarajan, Niranjan

doi:10.1038/s41591-020-0894-4

Cartography of opportunistic pathogens and antibiotic resistance genes in a tertiary hospital environment

Journal Article · Mon Jun 08 00:00:00 EDT 2020 · Nature Medicine

DOI:https://doi.org/10.1038/s41591-020-0894-4· OSTI ID:1766495

Chng, Kern Rei ^[1]; ^[1]; Bertrand, Denis ^[1]; Ng, Amanda Hui Qi ^[1]; Kwah, Junmei Samantha ^[1]; Low, Hwee Meng ^[1]; Tong, Chengxuan ^[1]; Natrajan, Maanasa ^[1]; Zhang, Michael Hongjie ^[1]; Xu, Licheng ^[2]; Ko, Karrie Kwan Ki ^[3]; Ho, Eliza Xin Pei ^[1]; Av-Shalom, Tamar V. ^[1]; Teo, Jeanette Woon Pei ^[4]; ^[1]; Chen, Swaine L. ^[1]; ^[5]; Ng, Oon Tek ^[6]; ^[7]; Ang, Brenda ^[8] more »

Genome Inst. of Singapore (Singapore)
Singapore Univ. of Technology and Design (Singapore)
Singapore General Hospital (Singapore); National Univ. of Singapore (Singapore). Graduate Medical School
National Univ. Hospital (Singapore)
Cornell Univ., Ithaca, NY (United States). Weill Medical College
National Centre for Infectious Diseases (Singapore); Tan Tock Seng Hospital (Singapore); Nanyang Technological Univ. (Singapore)
National Centre for Infectious Diseases (Singapore); Tan Tock Seng Hospital (Singapore); National Univ. of Singapore (Singapore)
National Centre for Infectious Diseases (Singapore); Tan Tock Seng Hospital (Singapore)
Genome Inst. of Singapore (Singapore); National Univ. of Singapore (Singapore)

Although disinfection is key to infection control, the colonization patterns and resistomes of hospital-environment microbes remain underexplored. We report the first extensive genomic characterization of microbiomes, pathogens and antibiotic resistance cassettes in a tertiary-care hospital, from repeated sampling (up to 1.5 years apart) of 179 sites associated with 45 beds. Deep shotgun metagenomics unveiled distinct ecological niches of microbes and antibiotic resistance genes characterized by biofilm-forming and human-microbiome-influenced environments with corresponding patterns of spatiotemporal divergence. Quasi-metagenomics with nanopore sequencing provided thousands of high-contiguity genomes, phage and plasmid sequences (>60% novel), enabling characterization of resistome and mobilome diversity and dynamic architectures in hospital environments. Phylogenetics identified multidrug-resistant strains as being widely distributed and stably colonizing across sites. Comparisons with clinical isolates indicated that such microbes can persist in hospitals for extended periods (>8 years), to opportunistically infect patients. These findings highlight the importance of characterizing antibiotic resistance reservoirs in hospitals and establish the feasibility of systematic surveys to target resources for preventing infections.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); US Naval Medical Research Center (NMRC); WorldQuant Foundation; Bill and Melinda Gates Foundation; Alfred P. Sloan Foundation

Contributing Organization:: MetaSUB Consortium

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1766495

Journal Information:: Nature Medicine, Journal Name: Nature Medicine Journal Issue: 6 Vol. 26; ISSN 1078-8956

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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The butterflies of a Cerrado–Atlantic Forest ecotone at Laguna Blanca reveal underestimation of Paraguayan butterfly diversity and need for conservation Dickens, Jeremy K.; McMahon, Leigh; Binnie, Sarah E. Journal of Insect Conservation, Vol. 23, Issue 4 https://doi.org/10.1007/s10841-019-00165-7	journal	July 2019
Climatic variables drive temporal patterns of α and β diversities of dung beetles Ferreira, S. C.; da Silva, P. G.; Paladini, A. Bulletin of Entomological Research, Vol. 109, Issue 3 https://doi.org/10.1017/S0007485318000676	journal	September 2018
Diversity-disease relationships and shared species analyses for human microbiome-associated diseases Ma, Zhanshan (Sam); Li, Lianwei; Gotelli, Nicholas J. The ISME Journal, Vol. 13, Issue 8 https://doi.org/10.1038/s41396-019-0395-y	journal	March 2019
A comprehensive non-redundant gene catalog reveals extensive within-community intraspecies diversity in the human vagina Ma, Bing; France, Michael T.; Crabtree, Jonathan Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14677-3	journal	February 2020
China’s tuberculosis epidemic stems from historical expansion of four strains of Mycobacterium tuberculosis Liu, Qingyun; Ma, Aijing; Wei, Lanhai Nature Ecology & Evolution, Vol. 2, Issue 12 https://doi.org/10.1038/s41559-018-0680-6	journal	November 2018
High frequency of shared clonotypes in human B cell receptor repertoires Soto, Cinque; Bombardi, Robin G.; Branchizio, Andre Nature https://doi.org/10.1038/s41586-019-0934-8	journal	February 2019
16S rDNA based skin microbiome data of healthy individuals and leprosy patients from India Bayal, Nitin; Nagpal, Sunil; Haque, Mohammed Monzoorul Scientific Data, Vol. 6, Issue 1 https://doi.org/10.1038/s41597-019-0232-1	journal	October 2019
Multi-marker metabarcoding approach to study mesozooplankton at basin scale Stefanni, Sergio; Stanković, David; Borme, Diego Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-30157-7	journal	August 2018
Gut microbiome modulation during treatment of mucositis with the dairy bacterium Lactococcus lactis and recombinant strain secreting human antimicrobial PAP Carvalho, Rodrigo; Vaz, Aline; Pereira, Felipe Luiz Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-33469-w	journal	October 2018
A multiscale study of fungal endophyte communities of the foliar endosphere of native rubber trees in Eastern Amazon Vaz, Aline B. M.; Fonseca, Paula L. C.; Badotti, Fernanda Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-34619-w	journal	November 2018
First report of community dynamics of arbuscular mycorrhizal fungi in radiocesium degradation lands after the Fukushima-Daiichi Nuclear disaster in Japan Higo, Masao; Kang, Dong-Jin; Isobe, Katsunori Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-44665-7	journal	June 2019
Female Blow Flies As Vertebrate Resource Indicators Owings, Charity G.; Banerjee, Aniruddha; Asher, Travis M. D. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-46758-9	journal	July 2019
Impact of coal mining on stream biodiversity in the US and its regulatory implications Giam, Xingli; Olden, Julian D.; Simberloff, Daniel Nature Sustainability, Vol. 1, Issue 4 https://doi.org/10.1038/s41893-018-0048-6	journal	April 2018
Dissecting macroecological and macroevolutionary patterns of forest biodiversity across the Hawaiian archipelago Craven, Dylan; Knight, Tiffany M.; Barton, Kasey E. Proceedings of the National Academy of Sciences, Vol. 116, Issue 33 https://doi.org/10.1073/pnas.1901954116	journal	July 2019
Global invasion history of the agricultural pest butterfly Pieris rapae revealed with genomics and citizen science Ryan, Sean F.; Lombaert, Eric; Espeset, Anne Proceedings of the National Academy of Sciences, Vol. 116, Issue 40 https://doi.org/10.1073/pnas.1907492116	journal	September 2019
Livin' on the edge: the importance of adjacent intermittent habitats in maintaining macroinvertebrate diversity of permanent freshwater marsh systems Boda, Pál; Móra, Arnold; Várbíró, Gábor Inland Waters, Vol. 8, Issue 3 https://doi.org/10.1080/20442041.2018.1461969	journal	July 2018
Investigating microbial indicators of anthropogenic marine pollution by 16S and 18S High-Throughput Sequencing (HTS) library analysis Buccheri, Maria Antonietta; Salvo, Eliana; Coci, Manuela FEMS Microbiology Letters, Vol. 366, Issue 14 https://doi.org/10.1093/femsle/fnz179	journal	July 2019
Triclosan-Selected Host-Associated Microbiota Perform Xenobiotic Biotransformations in Larval Zebrafish Weitekamp, Chelsea A.; Phelps, Drake; Swank, Adam Toxicological Sciences, Vol. 172, Issue 1 https://doi.org/10.1093/toxsci/kfz166	journal	September 2019
Specialization and niche overlap across spatial scales: Revealing ecological factors shaping species richness and coexistence in Australian songbirds Harmáčková, Lenka; Remešová, Eva; Remeš, Vladimír Journal of Animal Ecology, Vol. 88, Issue 11 https://doi.org/10.1111/1365-2656.13073	journal	July 2019
The role of livestock intensification and landscape structure in maintaining tropical biodiversity Alvarado, Fredy; Escobar, Federico; Williams, David R. Journal of Applied Ecology, Vol. 55, Issue 1 https://doi.org/10.1111/1365-2664.12957	journal	July 2017
Comparing convenience and probability sampling for urban ecology applications Speak, Andrew; Escobedo, Francisco J.; Russo, Alessio Journal of Applied Ecology, Vol. 55, Issue 5 https://doi.org/10.1111/1365-2664.13167	journal	May 2018
Low‐intensity management benefits solitary bees in olive groves Martínez‐Núñez, Carlos; Manzaneda, Antonio J.; Isla, Jorge Journal of Applied Ecology, Vol. 57, Issue 1 https://doi.org/10.1111/1365-2664.13511	journal	October 2019
Exotic eucalypts: From demonized trees to allies of tropical forest restoration? Brancalion, Pedro H. S.; Amazonas, Nino T.; Chazdon, Robin L. Journal of Applied Ecology, Vol. 57, Issue 1 https://doi.org/10.1111/1365-2664.13513	journal	October 2019
Bacterial colonization of minerals in grassland soils is selective and highly dynamic Vieira, Selma; Sikorski, Johannes; Gebala, Aurelia Environmental Microbiology, Vol. 22, Issue 3 https://doi.org/10.1111/1462-2920.14751	journal	August 2019
Environmental DNA analysis shows high potential as a tool for estimating intraspecific genetic diversity in a wild fish population Tsuji, Satsuki; Maruyama, Atsushi; Miya, Masaki Molecular Ecology Resources, Vol. 20, Issue 5 https://doi.org/10.1111/1755-0998.13165	journal	May 2020
How should we estimate diversity in the fossil record? Testing richness estimators using sampling‐standardised discovery curves Close, Roger A.; Evers, Serjoscha W.; Alroy, John Methods in Ecology and Evolution, Vol. 9, Issue 6 https://doi.org/10.1111/2041-210x.12987	journal	March 2018
The r package divDyn for quantifying diversity dynamics using fossil sampling data Kocsis, Ádám T.; Reddin, Carl J.; Alroy, John Methods in Ecology and Evolution, Vol. 10, Issue 5 https://doi.org/10.1111/2041-210x.13161	journal	March 2019
Choices of sampling method bias functional components estimation and ability to discriminate assembly mechanisms Lee, Roger H.; Guénard, Benoit Methods in Ecology and Evolution, Vol. 10, Issue 6 https://doi.org/10.1111/2041-210x.13175	journal	April 2019
Surveying tropical birds is much harder than you think: a primer of best practices Robinson, W. Douglas; Lees, Alexander C.; Blake, John G. Biotropica, Vol. 50, Issue 6 https://doi.org/10.1111/btp.12608	journal	October 2018
Canopy tree preference by insectivorous birds in shade‐coffee farms: Implications for migratory bird conservation Narango, Desirée L.; Tallamy, Douglas W.; Snyder, Kerry J. Biotropica, Vol. 51, Issue 3 https://doi.org/10.1111/btp.12642	journal	March 2019
Temporal variation in the influence of forest succession on caterpillar communities: A long‐term study in a tropical dry forest Boege, Karina; Villa‐Galaviz, Edith; López‐Carretero, Antonio Biotropica, Vol. 51, Issue 4 https://doi.org/10.1111/btp.12666	journal	May 2019
Quantifying regional biodiversity in the tropics: A case study of freshwater fish in Trinidad and Tobago Jones, Faith A. M.; Rutherford, Mike G.; Deacon, Amy E. Biotropica, Vol. 51, Issue 5 https://doi.org/10.1111/btp.12692	journal	August 2019
Elevational filtering and the evolution of planthoppers (Hemiptera, Fulgoromorpha) in Papua New Guinea Chatelain, Paul; Le Cesne, Maxime; Elias, Marianne Biotropica, Vol. 52, Issue 2 https://doi.org/10.1111/btp.12710	journal	March 2020
Linking dung beetle‐mediated functions to interactions in the Atlantic Forest: Sampling design matters Raine, Elizabeth H.; Mikich, Sandra B.; Lewis, Owen T. Biotropica, Vol. 52, Issue 2 https://doi.org/10.1111/btp.12722	journal	March 2020
Interpreting beta‐diversity components over time to conserve metacommunities in highly dynamic ecosystems Ruhí, Albert; Datry, Thibault; Sabo, John L. Conservation Biology, Vol. 31, Issue 6 https://doi.org/10.1111/cobi.12906	journal	May 2017
Recreational freshwater fishing drives non-native aquatic species richness patterns at a continental scale Davis, A. J. S.; Darling, J. A. Diversity and Distributions, Vol. 23, Issue 6 https://doi.org/10.1111/ddi.12557	journal	April 2017
Turnover and nestedness in subtropical dung beetle assemblages along an elevational gradient da Silva, Pedro G.; Lobo, Jorge M.; Hensen, Maristela C. Diversity and Distributions, Vol. 24, Issue 9 https://doi.org/10.1111/ddi.12763	journal	April 2018
Bees use anthropogenic habitats despite strong natural habitat preferences Collado, Miguel Á.; Sol, Daniel; Bartomeus, Ignasi Diversity and Distributions, Vol. 25, Issue 6 https://doi.org/10.1111/ddi.12899	journal	February 2019
The biodiversity benefit of native forests and mixed‐species plantations over monoculture plantations Wang, Xiaoyang; Hua, Fangyuan; Wang, Lin Diversity and Distributions, Vol. 25, Issue 11 https://doi.org/10.1111/ddi.12972	journal	August 2019
Differential temporal beta‐diversity patterns of native and non‐native arthropod species in a fragmented native forest landscape Matthews, Thomas J.; Sadler, Jon; Carvalho, Rui Ecography, Vol. 42, Issue 1 https://doi.org/10.1111/ecog.03812	journal	July 2018
Sampling design may obscure species–area relationships in landscape‐scale field studies Bueno, Anderson Saldanha; Masseli, Gabriel S.; Kaefer, Igor L. Ecography, Vol. 43, Issue 1 https://doi.org/10.1111/ecog.04568	journal	October 2019
Comparative responses of termite functional and taxonomic diversity to land‐use change Liu, Shengjie; Lin, Xiaobing; Behm, Jocelyn E. Ecological Entomology, Vol. 44, Issue 6 https://doi.org/10.1111/een.12755	journal	May 2019
Anthropogenic disturbance equalizes diversity levels in arbuscular mycorrhizal fungal communities García de León, David; Davison, John; Moora, Mari Global Change Biology, Vol. 24, Issue 6 https://doi.org/10.1111/gcb.14131	journal	April 2018
Trade‐offs between carbon stocks and biodiversity in European temperate forests Sabatini, Francesco Maria; de Andrade, Rafael Barreto; Paillet, Yoan Global Change Biology, Vol. 25, Issue 2 https://doi.org/10.1111/gcb.14503	journal	November 2018
Congruence across taxa and spatial scales: Are we asking too much of species data? Burrascano, S.; de Andrade, R. B.; Paillet, Y. Global Ecology and Biogeography, Vol. 27, Issue 8 https://doi.org/10.1111/geb.12766	journal	August 2018
Body size, reef area and temperature predict global reef‐fish species richness across spatial scales Barneche, D. R.; Rezende, E. L.; Parravicini, V. Global Ecology and Biogeography, Vol. 28, Issue 3 https://doi.org/10.1111/geb.12851	journal	December 2018
The acoustic ecology of an Amazonian bird assemblage: the role of allometry, competition and environmental filtering in the acoustic structure Torres, Ingrid M. D.; Barreiros, Marcelo H. M.; de Araújo, Carlos B. Ibis, Vol. 162, Issue 3 https://doi.org/10.1111/ibi.12720	journal	March 2019
Livestock areas with canopy cover sustain dung beetle diversity in the humid subtropical Chaco forest Guerra Alonso, Celeste Beatriz; Zurita, Gustavo A.; Bellocq, M. Isabel Insect Conservation and Diversity, Vol. 12, Issue 4 https://doi.org/10.1111/icad.12340	journal	January 2019
A cross-continental comparison of assemblages of seed- and fruit-feeding insects in tropical rain forests: Faunal composition and rates of attack Basset, Yves; Dahl, Chris; Ctvrtecka, Richard Journal of Biogeography, Vol. 45, Issue 6 https://doi.org/10.1111/jbi.13211	journal	March 2018
Model averaging fails to improve the extrapolation capability of the island species–area relationship Matthews, Thomas J.; Aspin, Thomas W. H. Journal of Biogeography https://doi.org/10.1111/jbi.13598	journal	June 2019
Genotypic diversity in root-endophytic fungi reflects efficient dispersal and environmental adaptation Glynou, Kyriaki; Ali, Tahir; Kia, Sevda Haghi Molecular Ecology, Vol. 26, Issue 18 https://doi.org/10.1111/mec.14231	journal	August 2017
Non‐random association patterns in a plant–mycorrhizal fungal network reveal host–symbiont specificity Sepp, Siim‐Kaarel; Davison, John; Jairus, Teele Molecular Ecology, Vol. 28, Issue 2 https://doi.org/10.1111/mec.14924	journal	May 2018
The roles of morphological traits, resource variation and resource partitioning associated with the dietary niche expansion in the fish‐eating bat Myotis pilosus Chang, Yang; Song, Shengjing; Li, Aoqiang Molecular Ecology https://doi.org/10.1111/mec.15127	journal	May 2019
Historical biome distribution and recent human disturbance shape the diversity of arbuscular mycorrhizal fungi Pärtel, Meelis; Öpik, Maarja; Moora, Mari New Phytologist, Vol. 216, Issue 1 https://doi.org/10.1111/nph.14695	journal	July 2017
Forest biomass, soil and biodiversity relationships originate from biogeographic affinity and direct ecological effects Noreika, Norbertas; Helm, Aveliina; Öpik, Maarja Oikos, Vol. 128, Issue 11 https://doi.org/10.1111/oik.06693	journal	July 2019
Reconciling biodiversity and carbon stock conservation in an Afrotropical forest landscape Van de Perre, Frederik; Willig, Michael R.; Presley, Steven J. Science Advances, Vol. 4, Issue 3 https://doi.org/10.1126/sciadv.aar6603	journal	March 2018
High Rate of Infection by Only Oncogenic Human Papillomavirus in Amerindians Vargas-Robles, Daniela; Magris, Magda; Morales, Natalia mSphere, Vol. 3, Issue 3 https://doi.org/10.1128/mSphere.00176-18	journal	June 2018
Vascular Epiphytic Diversity in a Neotropical Transition Zone Is Driven by Environmental and Structural Heterogeneity de la Rosa-Manzano, Edilia; Mendieta-Leiva, Glenda; Guerra-Pérez, Antonio Tropical Conservation Science, Vol. 12 https://doi.org/10.1177/1940082919882203	journal	January 2019
Probing the Rare Biosphere of the North-West Mediterranean Sea: An Experiment with High Sequencing Effort Crespo, Bibiana G.; Wallhead, Philip J.; Logares, Ramiro PLOS ONE, Vol. 11, Issue 7 https://doi.org/10.1371/journal.pone.0159195	journal	July 2016
Genetic structure and demographic inference of the regular sea urchin Sterechinus neumayeri (Meissner, 1900) in the Southern Ocean: The role of the last glaciation Díaz, Angie; Gérard, Karin; González-Wevar, Claudio PLOS ONE, Vol. 13, Issue 6 https://doi.org/10.1371/journal.pone.0197611	journal	June 2018
The menu varies with metabarcoding practices: A case study with the bat Plecotus auritus Andriollo, Tommy; Gillet, François; Michaux, Johan R. PLOS ONE, Vol. 14, Issue 7 https://doi.org/10.1371/journal.pone.0219135	journal	July 2019
Successional, spatial, and seasonal changes in seed rain in the Atlantic forest of southern Bahia, Brazil Piotto, Daniel; Craven, Dylan; Montagnini, Florencia PLOS ONE, Vol. 14, Issue 12 https://doi.org/10.1371/journal.pone.0226474	journal	December 2019
Molecular sequencing and morphological identification reveal similar patterns in native bee communities across public and private grasslands of eastern North Dakota Darby, Brian; Bryant, Russ; Keller, Abby PLOS ONE, Vol. 15, Issue 1 https://doi.org/10.1371/journal.pone.0227918	journal	January 2020
Simple does not mean poor: grasslands and forests harbor similar ant species richness and distinct composition in highlands of southern Brazil Klunk, Cristian Luan; Giehl, Eduardo Luís Hettwer; Lopes, Benedito Cortês Biota Neotropica, Vol. 18, Issue 3 https://doi.org/10.1590/1676-0611-bn-2017-0507	journal	January 2018
Cervicovaginal Fungi and Bacteria Associated With Cervical Intraepithelial Neoplasia and High-Risk Human Papillomavirus Infections in a Hispanic Population Godoy-Vitorino, Filipa; Romaguera, Josefina; Zhao, Chunyu Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02533	journal	October 2018
Comparative Analysis of Intestine Microbiota of Four Wild Waterbird Species Laviad-Shitrit, Sivan; Izhaki, Ido; Lalzar, Maya Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01911	journal	August 2019
Antibiotic-Induced Perturbations Are Manifested in the Dominant Intestinal Bacterial Phyla of Atlantic Salmon Gupta, Shruti; Fernandes, Jorge; Kiron, Viswanath Microorganisms, Vol. 7, Issue 8 https://doi.org/10.3390/microorganisms7080233	journal	August 2019
Relationship between Wetland Plant Communities and Environmental Factors in the Tumen River Basin in Northeast China Zheng, Xiaojun; Fu, Jing; Ramamonjisoa, Noelikanto Sustainability, Vol. 11, Issue 6 https://doi.org/10.3390/su11061559	journal	March 2019
A meta-barcoding census of freshwater planktonic protists in Appalachia – Natural Tunnel State Park, Virginia, USA Cahoon, A. Bruce; Huffman, Ashley G.; Krager, Megan M. Metabarcoding and Metagenomics, Vol. 2 https://doi.org/10.3897/mbmg.2.26939	journal	October 2018
Stuck amongst introduced species: Trophic ecology reveals complex relationships between the critically endangered Niau kingfisher and introduced predators, competitors and prey Zarzoso-Lacoste, Diane; Bonnaud, Elsa; Corse, Emmanuel NeoBiota, Vol. 53 https://doi.org/10.3897/neobiota.53.35086	journal	December 2019
Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics Kavagutti, Vinicius S.; Andrei, Adrian-Ştefan; Mehrshad, Maliheh BioMed Central https://doi.org/10.5167/uzh-183761	text	January 2019
Variegated tropical landscapes conserve diverse dung beetle communities Costa, Cristiane; Oliveira, Victor Hugo F.; Maciel, Rafaella PeerJ, Vol. 5 https://doi.org/10.7717/peerj.3125	journal	January 2017
Nectar-living yeasts of a tropical host plant community: diversity and effects on community-wide floral nectar traits Canto, Azucena; Herrera, Carlos M.; Rodriguez, Rosalina PeerJ, Vol. 5 https://doi.org/10.7717/peerj.3517	journal	January 2017
Cover cropping can be a stronger determinant than host crop identity for arbuscular mycorrhizal fungal communities colonizing maize and soybean Higo, Masao; Tatewaki, Yuya; Gunji, Kento PeerJ, Vol. 7 https://doi.org/10.7717/peerj.6403	journal	January 2019
A highly diverse fungal community associated with leaves of the mangrove plant Acanthus ilicifolius var. xiamenensis revealed by isolation and metabarcoding analyses Chi, Wei-Chiung; Chen, Weiling; He, Chih-Chiao PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7293	journal	January 2019

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