The Bat Microbiome Project This project seeks to improve our knowledge of the relationships between bats and their bacterial and fungal symbionts, using a broad range of molecular and imaging tools. Initial sampling for this work has focused primarily in the East African countries of Uganda and Kenya, transecting a broad range of ecosystems and habitat types. These samples provide baseline data for a large number of bat species with diverse life histories, and are allowing us to examine the effects of anthropogenic disturbance and unnatural habitat selection on chiropteran symbionts - including parasites, and pathogens. We are also addressing the extent to which bats exhibit patterns of phylosymbiosis with their symbionts, and whether the skin microbiome influences rates of ectoparasitism and malaria in Afrotropical bats.
In collaboration with the Marine Biological Laboratory (Woods Hole, MA), colleagues and I are exploring the diversity of bacterial symbionts associated with cephalopods maintained in culture. Using 16S rRNA sequencing and fluorescence in situ hybridization, we identified a highly simplified microbiome in the European common cuttlefish, Sepia officinalis, comprising a single dominant Vibrio amplicon sequence variant (ASV) in the gastrointestinal tract of captive animals and a single dominant ASV in the family Piscirickettsia associated with the gills. We are now expanding this survey to include additional cephalopod species at MBL, as well as wild-caught individuals (and potentially some deep-sea dwellers, stay tuned!), and are developing type cultures in the process with the goal of expanding the experimental toolkit for this highly promising system.
Ecology & Evolution of Malarial Parasites Malaria parasites affect nearly all terrestrial vertebrates, and their impact on vertebrate hosts ranges from mild to severe, in some cases leading to extinction of entire species. Advances in molecular methods have revealed an astonishing degree of diversity among malaria parasites and closely-related haemosporidia, and host switching has occurred frequently throughout their evolutionary history. Without an accurate account of parasite diversity, we may only guess at the evolutionary history underlying current relationships. My research has focused primarily in the east African tropics, but has included Neotropical parasites as well. I use phylogenetic and comparative genomic approaches to resolve evolutionary relationships between malaria parasites of birds and mammals, and to explore the factors leading to diversification and host switching in haemosporidian parasites.
Micrographs of blood stage gametocytes of bat haemosporidians: (A-C) Hepatocystis cf. epomophori macrogametocytes ex. Epomops franquetti; (D-E) Polychromophilus melanipherus microgametocytes and (F) macrogametocyte ex. Miniopterus natalensis; (G-H) Nycteria sp. microgametocyte, (I) macrogametocyte, and (J) gametocyte ex. Hipposideros cyclops.
Host life history and malarial parasite infection Prevalence and host-specificity of malaria parasites are highly variable across avian taxa. By comparing rates of parasitism across a broad range of bird species, we were able to assess the extent to which host life history traits and ecological factors are linked to infection by Plasmodium, Haemoproteus, or Leucocytozoon. To study the relationship between host traits and probability of haemosporidian infection, colleagues and I examined a broad range of bird species from 16 avian orders in Northern Malawi, discovering over 200 new parasite lineages in the process. This study was the first to test such associations in Afrotropical birds. This work is in collaboration with the Cornell Lab of Ornithology, Field Museum of Natural History, and University of North Dakota.
Phylogenetics of malarial parasites and closely related haemosporidia
To identify and describe malaria parasite diversity, I have sequenced the mitochondrial cytochrome b gene. While useful for differentiation between parasite lineages (see MalAvi database), this marker does not provide sufficient data for resolution of relationships between most lineages of avian malaria (Plasmodium and Haemoproteus). To address this I collectied additional data from nuclear and apicoplast genomes, allowing improved phylogentic resolution for a diverse assemblage of malaria parasites I have identified in east African vertebrates.
Among the many African mammals I have tested, bats have proven to be consistent hosts of haemosporidian parasites - most of which represent new genetic lineages, and possibly new species. I continue to collect samples for haemosporidian analysis as I carry out my work on bats.
Laser capture and comparative genomics of Plasmodium parasites
Currently there are few publicly available genomes of Plasmodium parasites (see PlasmoDB), with no representation of avian Plasmodium species. My colleagues and I have used laser capture microdissection microscopy (LCMM) methods to obtain parasite isolates from birds for genomic sequencing and comparative analyses. Although this study recovered only a small fraction of genomic material, we were able to demonstrate that LCMM paired with whole genome amplification methods is a viable option for obtaining genomic material for comparative genomic analyses and the development of phylogenetic markers.
In Review Lutz, H. L., Vangelatos A., Gottel N., Osculati A., Visona S., Finley S. J., Tuomisto S., Karhunen P., Gilbert J. A., T. Javan G. T. In Review. Manner of death and demographic effects on microbial community composition in organs of the human cadaver
Fecchio, A., Bosholn, M., Bell, J. A., Lutz, H. L., Cueto, V. R., González-Acuña, D., Vaughan, J. A., Stromlund, C., Kvasager, D., Pinho, J. B., Berv, J, Anciães, M., Zyskowski, K., Dispoto, J. H., Tkach, V. V., Weckstein, J. D. In Review. Diversity and distributions of Leucocytozoon in New World birds.
(15) Song, S. J., Sanders, J., Delsuc, F., Metcalf, J. Amato, K., Taylor, M. W., Mazel, F., Lutz, H. L., Winker, K., Graves, G. R., Humphrey, G., Gilbert, J. A., Hackett, S. J., White, K. P., Skeen, H. R., Kurtis, S. M., Withrow, J., Braile, T., Miller, M., McCracken, K., Maley, J., Blanton, J. M., McKenzie, V. J., Knight, R. In Press. Comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats. mBio. doi:10.1128/mBio.02901-19 PDF
(14) Lutz, H. L., Jackson E. W., Webala, P. W., Babyesiza, W. S., Kerbis Peterhans, J. C., Demos, T. C., Patterson, B. D., Gilbert, J. A. 2019. Ecology and host identity outweigh evolutionary history in shaping the bat microbiome. mSystems. doi:10.1128/mSystems.00511-19 PubMed, PDF
(13) Demos T. C., Webala P. W., Lutz, H. L., Kerbis Peterhans J. C., Goodman S. M., Cortés-Delgado N., Bartonjo M., Patterson B. D. 2019. Molecular systematics and coalescent delimitation of a cryptic radiation of African long-fingered bats (Chiroptera, Miniopteridae). Zoologica Scripta. doi:10.1111/zsc.12388 PDF
(12) Fecchio, A., Bell, J., Bosholn, M., Vaughan, J., Tkach, V., Lutz, H. L.; Cueto, V., Gorosito, C., González-Acuña, D., Stromlund, C., Kvasager, D., Comiche, K., Kirchgatter, K., Pinho, J., Berv, J., Anciaes, M., Fontana, C., Zyskowski, K., Sampaio, S., Dispoto, J., Galen, S., Weckstein, J. D., Clark, N. 2019. An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds. Journal of Animal Ecology. doi:10.1111/1365‐2656.13117 PubMed, PDF
(11) Phillips C. D., Dunnum J. L., Dowler R. C., Bradley L. C., Garner H. J., MacDonald K. A., Lim B.K., Revelez M. A., Campbell M. L., Lutz, H. L., Cook J. A., Bradley R. D., and the Systematic Collections Committee of the American Society of Mammalogists. 2019. Curatorial guidelines and standards of the American Society of Mammalogists for collections of genetic resources. Journal of Mammalogy, 100(6), 1690-1694. PDF
(10) Lutz, H. L., Ramírez-Puebla T., Abbo L., Durand A., Schlundt C., Sjaarda A. K., Gottel N., Hanlon R. T., Gilbert J. A., Mark Welch J. L. 2019. A simple microbiome in the European common Cuttlefish, Sepia officinalis. mSystems.00177-19. PubMed, PDF
(9) Fecchio, A., Bell, J.A., Pinheiro, R., Cueto, V., Gorosito, C., Lutz, H.L., Gaiotti, M., Paiva, L., França, L., Toledo-Lima, G., Tolentino, M., Pinho, J., Tkach, V., Fontana, C., Grande, J., Santillán, M., Caparroz, R., Roos, A., Bessa, R., Nogueira, W., Moura, T., Nolasco, E., Comiche, K., Kirchgatter, K., Guimarães, L., Dispoto, J., Marini, M., Weckstein, J.D., Batalha-Filho, H., Collins, M. D. 2019. Avian host composition, local speciation, and dispersal drive the regional assembly of avian malaria parasites in South American birds. Molecular Ecology, 28(10), 2681-2693. PubMed,PDF
(7) Fecchio, A., Wells, K., Bell, J. A., Tkach, V. V., Lutz, H. L., Weckstein, J. D., Clegg, S. M., Clark, N. J. 2019.Climate variation influences host specificity in avian malaria parasites. Ecology Letters, 22(3), 547-557. PubMed, PDF
(6) Lutz, H. L., Carryl, S., Santymire, R. M. 2019.Wildlife Microbial Genomics and Endocrinology. In D. Marco (editor). Microbial Ecology: Current advances from genomics, metagenomics, and other “omics” approaches. Caister Academic Press, Poole, UK. Order Book
(5) Lutz, H. L., Tkach, V. T., Weckstein, J. D. 2017. Methods for Specimen-based Studies of Avian Symbionts. Pp. 157-183 in M. S. Webster (editor). The Extended Specimen: Emerging Frontiers in Collections-based Ornithological Research. Studies in Avian Biology (no. 50). CRC Press, Boca Raton, FL. Order Book, PDF
(4) Lutz, H. L., Marra, N. J., Grewe, F., Carlson, J., Palinauskas, V. Valkiūnas, G., Stanhope, M. J. 2016. Laser capture microdissection microscopy and next generation genome sequencing of the avian malaria parasite, Plasmodium relictum. Parasitology Research, 115(12), 4503-4510. PubMed, PDF (3) Lutz, H. L., Patterson, B. D., Kerbis, J. C., Webala, P. W., Stanley, W. T., Gnoske, T. P., Hackett, S. J., Stanhope, M. J. 2016. Diverse sampling of East African haemosporidians reveals chiropteran origin of malaria parasites in primates and rodents. Molecular Phylogenetics and Evolution, 99, 7-15. PubMed, PDF
(2) Lutz, HL, Hochachka, WM, Engel, JI, Bell, JA, Tkach, VV, Bates, JM, Hackett, SJ, Weckstein, JD. 2015. Parasite prevalence corresponds to host life history in a diverse assemblage of Afrotropical birds and haemosporidian parasites. PLoS ONE doi:10.1371/journal/pone.012154. PubMed, PDF 2013
(1) Lutz, HL, Weckstein, JD, Patané, JL, Bates, JM, Aleixo, A. 2013. Biogeography and spatio-temporal diversification of Selenidera and Andigena toucans (Aves:Ramphastidae). Molecular Phylogenetics and Evolution, 69, 873 – 883. PubMed, PDF
Awards & Support
2017 - 2018 NSF Postdoctoral Research Fellowship in Biology 2015 - pres. Edward A. Bouchet Graduate Honor Society Fellow 2014 - 2015 Lester Armour and William A. & Stella M. Rowley Fellow, Field Museum of Natural History 2013 - 2016 NSF Graduate Research Fellowship 2011 - 2012 Presidential Life Sciences Fellowship, Cornell University
2018 Council on Africa, Field Museum of Natural History 2016 Council on Africa, Field Museum of Natural History 2015 Athena Fund, Cornell Lab of Ornithology 2014 Cornell Center for Comparative and Population Genomics 2014 Cornell College of Agriculture and Life Sciences Alumni Grant 2014 Next Gen/Illumina Grant, Pritzker Laboratory of Molecular Systematics and Evolution 2013 Athena Fund, Cornell Lab of Ornithology 2013 American Society of Naturalists 2013 NSF Malaria Research Coordination Network 2012 NSF Malaria Research Coordination Network 2012 Andrew W. Mellon Grant 2012 Sigma Xi, Cornell Chapter 2011 Krammer Graduate Research Grant