Univ.-Prof. Dr. Alexander Loy

Professor
University of Vienna
Department of Microbiology and Ecosystem Science
Division of Microbial Ecology
Althanstr. 14
A-1090 Vienna
Phone: +43 1 4277 76605
Austria

Sulfur microorganisms

The sulfur cycle is one of the oldest biogeochemical cycles on Earth and it is mainly through microbial activities that the sulfur cycle is intimately intertwined with the cycling of other elements such as carbon or nitrogen. My group is interested in the evolution of sulfur microorganisms, their yet largely unexplored diversity, distribution, and ecological function in various environments, and their roles as symbionts of animals and humans.

Sulfate-reducing cellWe are investigating the evolution of sulfur microorganisms by comparative phylogenetic analysis of key genes such as dsrAB, encoding dissimilatory (bi)sulfite reductase and, more recently, by phylogenomics. We specifically aim to reveal the ecology and biogeography of sulfate-reducing microorganisms in globally relevant anoxic ecosystems such as the ocean floor and terrestrial wetlands. Isotope-labeling techniques allow us to show how the physiological interactions of individual members of complex microbial communities influence important processes in the global carbon and sulfur cycles such as degradation of organic matter and greenhouse gas emissions. We further use genomics and targeted metagenomic approaches to get insights into the genome evolution and metabolism of ecologically important sulfur microorganisms such as rare, sulfate-reducing Desulfosporosinus species in wetlands (Pester et al. 2012). 

Intestinal microbiota

The symbiotic intestinal microbiota provides important benefits to its animal and human host such as breakdown of complex nutritional substrates and protection against pathogens. Changes in the intestinal microbiota are, however, associated with many diseases. We are interested in the ecophysiology of the gut microbiota in health and disease. In the context of various diseases such as inflammatory bowel disease, cancer or intestinal infections, we specifically aim to answer how nutrition impacts the gut microbiota and which/how individual community members influence physiology and health of their host.

Individual cells of the intestinal microbiota either compete for substrates due to functional overlap or cooperate in syntrophic substrate degradation, resulting in a dynamic network of synergistic and antagonistic physiological interactions that are reciprocally influenced by the fluctuating physical and chemical environment of the gut. Here, in particular single cell isotope labeling tools promise yet unavailable detailed insights into host- or diet-derived substrate partitioning and niche competition among individual intestinal microbiota members, including incoming pathogens (Stecher, Berry, and Loy, 2013).

One focus of our work is the evolution and function of sulfur compounds-utilizing gut microorganisms because a balanced sulfur metabolism is crucial for intestinal homeostasis and host health. Furthermore, some pathogens such as Salmonella influence the intestinal sulfur metabolism to selectively support their outgrowth and fitness, but the role of the indigenous sulfur microbiota during these intestinal infections is unknown.

Techniques

To accomplish our research goals, we use a holistic approach that combines molecular biology, genomic, and isotope-labeling techniques such as highly parallel amplicon next-generation-sequencing of functional and phylogenetic marker genes, genomics and postgenomic analyses (meta-omics) of isolates and complex communities, DNA microarrays, fluorescence in situ hybridization, real-time PCR, Raman microspectroscopy, NanoSIMS, and phylogenetics.

Together with other DOME members, we are continuously developing novel molecular and isotope-labeling methods for structure-function analysis of complex microbial communities.

Research Topics

  • Evolution and ecology of sulfur microorganisms, with focus on sulfate-reducing microorganisms
  • Function of the intestinal microbiota in health and disease
  • Development of molecular and isotope-labeling methods for studying uncultivated microorganisms in their natural environment

PUBLICATIONS

See here for a complete list of peer-reviewed papers, book chapters, and other publications.

CURRENT PROJECTS

JOINING THE TEAM

Information on open research positions can be found here. If you are interested in joining our team with your own fellowship, please check out our PhD & postdoc program and get in touch with Alex for details.

Recent projects

Intestinal microbiota - Inflammation and a new method for analysis of microbial physiology in vivo

Inflammatory bowel diseases are characterized by an altered gut microbiota composition. By using mouse colitis models, we identified indicator phylotypes for health state (Berry et al. 2012Berry et al. 2015) and revealed characteristic changes in the microbial transcriptome and interactions with the host (Schwab et al. 2014). In a clinical pilot study, we showed that treatment success and the temporal fecal microbiota dynamics varied among ulcerative colitis patients after receiving fecal microbiota transplantation from healthy donors as an intervention therapy (Angelberger et al. 2013). By developing a novel single-cell, isotope-probing method, we could identify, for the first time, important foragers of mouse host-derived protein compounds in vivo and show that the host-foraging phenotype of these bacteria is quantitatively dependent on the complexity of the intestinal microbiota (Berry et al. 2013Stecher et al. 2013).

Selected publications on this theme:

  • Berry D, Kuzyk O, Rauch I, Heider S, Schwab C, Hainzl E, Decker T, Müller M, Strobl B, Schleper C, Urich T, Wagner M, Kenner L, Loy A. 2015. Intestinal microbiota signatures associated with inflammation history in mice experiencing recurring colitis. Front Microbiol. 6: 1408.
  • Schwab C, Berry D, Rauch I, Rennisch I, Ramesmayer J, Hainzl E, Heider S, Decker T, Kenner L, Müller M, Strobl B, Wagner M, Schleper C, Loy A, Urich T. 2014. Longitudinal study of murine microbiota activity and interactions with the host during acute inflammation and recovery. ISME J. 8: 1101-1114.
  • Berry D, Stecher B, Schintlmeister A, Reichert J, Brugiroux S, Wildd B, Wanek W, Richter A, Rauch I, Decker T, Loy A, Wagner M. 2013. Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing. Proc. Natl. Acad. Sci. USA 110: 4720-4725.
  • Stecher B, Berry D, Loy A. 2013. Colonization resistance and microbial ecophysiology: Using gnotobiotic mouse models and single-cell technology to explore the intestinal jungle. FEMS Microbiol. Rev. 37: 793-829.
  • Angelberger S, Reinisch W, Makristathis A, Lichtenberger C, Dejaco C, Papay P, Novacek G, Trauner M, Loy A, Berry D. 2013. Temporal bacterial community dynamics vary among ulcerative colitis patients after fecal microbiota transplantation. Am. J. Gastroenterol. 108: 1620-1630.
  • Berry D, Schwab C, Milinovich G, Reichert J, Ben Mahfoudh K, Decker T, Engel M, Hai B, Hainzl E, Heider S, Kenner L, Müller M, Rauch I, Strobl B, Wagner M, Schleper C, Urich T, Loy A. 2012. Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis. ISME J. 6: 2091-106.

 

Sulfate-reducing microorganisms mitigate methane emissions from wetlands

Wetlands are important carbon sinks but at the same time major global sources of the greenhouse gas methane. A hidden sulfur cycle in wetlands allows sulfate-reducing microorganism to successfully compete with methanogenic archaea and thereby to reduce methane emissions (Pester et al. 2012). While novel, uncultivated lineages dominate dsrAB diversity in wetlands (Steger et al. 2011), we identified rare microbiota members (including Desulfosporosinus) as important sulfate reducers in an acidic peatland by comparative 16S rRNA gene- and dsrAB-stable isotope probing (Pester et al. 2010). To further our understanding of sulfate reducer ecophysiology and genomics in peatlands, we are currently investigating the species interactions (Hausmann et al. 2016) and metatranscriptome dynamics in microcosms under in situ-like conditions.

Selected publications on this theme:

  • Hausmann B, Knorr K-H, Schreck K, Tringe SG, del Rio TG, Loy A, and Pester M [2016] Consortia of low-abundance bacteria drive sulfate reduction-dependent degradation of fermentation products in peat soil microcosms. ISME J. doi: 10.1038/ismej.2016.42
  • Pester M, Knorr K-H, Friedrich MW, Wagner M, Loy A. 2012. Sulfate-reducing microorganisms in wetlands - fameless actors in carbon cycling and climate change. Frontiers Microbiol. 3: 72.
  • Steger D, Wentrup C, Braunegger C, Deevong P, Hofer M, Richter A, Baranyi C, Pester M, Wagner M, Loy A. 2011. Microorganisms with novel dissimilatory (bi)sulfite reductase genes are widespread and part of the core microbiota in low-sulfate peatlands. Appl. Environ. Microbiol. 77: 1231-1242.
  • Pester M, Bittner N, Deevong P, Wagner M, Loy A. 2010. A 'rare biosphere' microorganism contributes to sulfate reduction in a peatland. ISME J. 12: 1591-1602.

 

Evolution and environmental diversity of an ancient enzyme - dissimilatory (bi)sulfite reductase

The evolution of DsrAB-type dissimilatory sulfite reductase has been influenced by surprisingly few lateral gene transfer and gene duplication events, which makes this enzyme and its genes, within certain limits, useful diagnostic markers for environmental studies of sulfite/sulfate-reducing and some sulfur-oxidizing microorganisms (Sabehi et al. 2005, Loy et al. 2009, Gruber-Vodicka et al. 2011). A recent phylogenetic and environmental meta-analysis of all available dsrAB sequences identified more than 13 family-level lineages without any cultivated representatives, suggesting that major taxa of sulfite/sulfate-reducing microorganisms have not yet been identified (Müller et al. 2015). Our publically available dsrAB/DsrAB database, a new multi-level classification system, and new primers now allow for large-scale dsrAB ecology studies using multiplex amplicon sequencing (Pelikan et al. 2016).

Notably, abundant ocean viruses also carry microbial sulfur genes and potentially manipulate the sulfur metabolism of their microbial hosts (Roux et al. 2016).

Selected publications on this theme:

  • Roux S, Brum JR, Dutilh BE, Sunagawa S, Duhaime MB, Loy A, Poulos BT, Solonenko N, Lara E, Poulain J, Pesant S, Kandels-Lewis S, Dimier C, Picheral M, Searson S, Cruaud C, Alberti A, Duarte CM, Gasol JM, Vaque D, Tara Oceans Coordinators, Bork P, Acinas SG, Wincker P, and Sullivan MB. 2016. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature. 537: 689–693. doi: 10.1038/nature19366
  • Pelikan C, Herbold CW, Hausmann B, Müller AL, Pester M, Loy A. 2016. Diversity analysis of sulfite- and sulfate-reducing microorganisms by multiplex dsrA and dsrB amplicon sequencing using new primers and mock community-optimized bioinformatics. Environ Microbiol. doi: 10.1111/1462-2920.13139
  • Müller AL, Kjeldsen KU, Rattei T, Pester M, Loy A. 2015. Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi)sulfite reductases. ISME J. 9: 1152-1165.
  • Gruber-Vodicka HR, Dirks U, Leisch N, Baranyi C, Stoecker K, Bulgheresi S, Heindl NR, Horn M, Lott C, Loy A, Wagner M, Ott J. 2011. Paracatenula, an ancient symbiosis between thiotrophic Alphaproteobacteria and catenulid flatworms. Proc. Natl. Acad. Sci. USA 108: 12078-12083.
  • Loy A, Duller S, Baranyi C, Mußmann M, Ott J, Sharon I, Béjà O, Le Paslier D, Dahl C, Wagner M. 2009. Reverse dissimilatory sulfite reductase as phylogenetic marker for a subgroup of sulfur-oxidizing prokaryotes. Environ. Microbiol. 11: 289-299.
  • Sabehi G#, Loy A#, Jung KH, Partha R, Spudich JL, Isaacson T, Hirschberg J, Wagner M, Beja O. 2005. New insights into metabolic properties of marine bacteria encoding proteorhodopsins. PLoS Biol. 3: e273. #equal contribution

 

Dormant microbes provide clues about passive dispersal of microorganisms in the ocean

The combined effects of passive dispersal and environmental selection influence microbial biogeography, but the contribution of either factor is difficult to discern. Inactive spores of thermophilic bacteria that are present in the cold seabed are not subject to environmental selection and thus ideal dispersal indicators (Hubert et al. 2009, de Rezende et al. 2013). These spore-forming microorganisms likely originate from hot anoxic environments in the sea floor or the ocean crust such as hydrothermal vents and their overlying sediments, or gas and oil reservoirs. We showed that individual phylotypes of thermophilic spores have various patterns of spatial distribution in the world oceans and were dispersal limited to different degrees. The overall distribution pattern of thermophilic spores suggests that the impact of passive dispersal on marine microbial biogeography is controlled by the connectivity of local water masses to ocean circulation (Müller et al. 2014).

Selected publications on this theme:

  • Müller AL, de Rezende JR, Hubert C, Kjeldsen KU, Lagkouvardos I, Berry D, Jørgensen BB, Loy A. 2014. Endospores of thermophilic bacteria as tracers of microbial dispersal by ocean currents. ISME J. 8: 1153-1165.
  • de Rezende JR, Kjeldsen KU, Hubert C, Finster K, Loy A, Jørgensen BB. 2013. Dispersal of thermophilic Desulfotomaculum endospores to Baltic Sea sediments over thousands of years. ISME J. 7: 72-84.
  • Hubert C, Loy A, Nickel M, Arnosti C, Baranyi C, Brüchert V, Ferdelman T, Finster K, Christensen FM, Rosa de Rezende J, Vandieken V, Jørgensen BB. 2009. A constant flux of diverse thermophilic bacteria into the cold Arctic seabed. Science 325: 1541-1544.