Bacteria and Archaea constitute the overwhelming majority of genetic and metabolic diversity on this planet. To understand these organisms in their native habitats, environmental microbiologists are tasked with two fundamental questions. First, how do ecological and evolutionary processes (e.g., environmental gradients, symbiosis, competition, recombination, natural selection) create and structure genetic diversity? Second, how is this genetic diversity linked to the diverse biogeochemical functions of microorganisms in nature?

Our research explores these questions for marine microorganisms, using the tools of genomics and molecular biology. We are particularly interested in how marine microbial diversity, genome evolution, and physiology are structured by environmental gradients, notably dissolved oxygen concentration, as well as by interactions with other organisms (through symbioses for example).

A primary focus of the lab is to understand microbial communities in marine oxygen minimum zones (OMZs) - see below. These microbially-dominated ecosystems support functionally diverse but under-characterized communities of bacteria, archaea, and microbial eukaryotes whose metabolisms play critical roles in global biogeochemical cycles. We also study marine symbioses between bacteria and other organisms, including marine invertebrates. Some symbiotic bacteria are closely related to major clades of free-living OMZ bacteria. These groups are therefore natural systems for exploring the role of symbiosis in structuring bacterial genome content and ecology.

Our research integrates the broad fields of marine biology, microbiology, and molecular evolution and genomics. This work has both descriptive and experimental components, and involves a blend of field, molecular, and bioinformatic techniques, the latter focused (primarily) on the analysis of high-throughput sequence datasets. We welcome inquiries from potential students, post-docs, and collaborators who share these interests. Current lab members include students of both the Biology Ph.D. program at Georgia Tech, as well as the Bioinformatics Ph.D. program.

Oxygen minimum zones

Global distribution of marine oxygen minimum zones. Map shows the minimum values of water column dissolved oxygen concentrations (< 50 uM). Data are from the World Ocean Atlas.

A major challenge for earth scientists is to understand how oceans respond to decreasing oxygen levels. Areas of low oxygen, oxygen minimum zones (OMZs), are predicted to increase in both expanse and frequency in response to climate warming and human modifications of coastal zones. Such shifts have profound consequences for biogeochemical cycles, as OMZs are critical sites for microbially-mediated transformations of carbon, nitrogen, and sulfur, including releases of key greenhouse gases (e.g., N2O). OMZs occur throughout the world's ocean but vary substantially in biological, chemical, and physical properties, notably the levels of primary production and oxygen availability (for a review, see Ulloa et al. 2012, PNAS, 109: 15996-16003). How this variation differentially structures microbial taxonomic composition, population-level genomic subdivision, and metabolic processes is poorly understood. This is due in part to a lack of genomic and metagenomic (community DNA) data enabling comparisons across diverse low-oxygen systems.

Our research uses genomics, meta-omics (see below), and physiological measurements to explore microbial diversity and metabolism across a range of low-oxygen systems, with a particular emphasis on OMZ bacteria that use inorganic sulfur or methane compounds for energy metabolism. Sulfur- and methane-based metabolism in OMZs also has direct implications for coupled nitrogen and carbon cycling. Specifically, we study pelagic microbial communities in two prominent end-members in the spectrum of OMZ types, the permanent anoxic OMZs (AMZs) of the Eastern Tropical Pacific Ocean where O2 can fall below detection (< 15 nM), and the seasonally hypoxic “deadzone” in the Gulf of Mexico (GoM; O2 < 20 uM).

Research at these sites is funded by generous grants from the US National Science Foundation (awards 1151698 and 1558916), the Alfred P. Sloan Foundation and the Department of Energy Community Science Program. This work has thus far involved cruises to the GoM (2012) and the Eastern Tropical North Pacific (ETNP) AMZ south of Baja California (2013,2014), with additional work scheduled for 2015. These field campaigns have involved participants at all levels of scientific training (undergraduate to senior PI), collaborations from multiple US and international institutions, and cross-disciplinary sampling and analytical approaches. Our work at these sites, notably the ETNP AMZ, is designed to complement existing research efforts at these and at other oceanographically diverse OMZ sites. A broad goal of this research is to facilitate interactions among diverse communities (oceanographers, microbial scientists, geochemists) to develop an integrated understanding of marine ecosystem response to oxygen depletion and climate change.

Microbial Symbiosis

Symbiosis, defined broadly as a long-term interaction between species, is among the most pervasive evolutionary and ecological strategies in marine ecosystems, impacting fundamental processes such as speciation, ecosystem structuring, primary production, nutrient cycling, and disease. Marine microbial symbioses span a striking diversity of hosts and symbionts from all three Domains of life. These associations vary widely in key biological factors, including the extent to which symbionts affect host fitness (e.g., mutualism vs. commensalism vs. parasitism), integrate into host tissue, and exchange genetic material with free-living microorganisms. Though such factors have been explored for certain well-studied associations, most marine symbioses remain understudied.

Our research explores the diversity, evolution, and function of symbioses between bacteria and animals. We focus primarily on marine symbioses, notably associations between deep-sea invertebrates and intracellular chemoautotrophic bacteria that fix carbon for their hosts. We also study associations involving complex multi-species microbiomes, such as the diverse communities of bacteria in vertebrate guts and epidermal layers. Such microbiomes contain tens to hundreds of interacting species, often with complex effects on host development, health, and behavior. We employ genomic and meta-omic methods to study these associations, often in collaboration with biogeochemists and ecologists.

This work addresses broad questions: How do symbionts or microbiomes affect host physiology and ecology? How does symbiont genome evolution and metabolism vary in response to symbiont transmission mode and the level of symbiont-host specificity (e.g., free-living versus host-associated lineages)? How are symbiont and host diversity structured within and across populations and in response to factors external to the symbiosis, such as environmental habitat heterogeneity and the genetic composition of the free-living microbial community? Answering these questions for diverse associations sheds light on the role of symbiosis as a driver of biological innovation and ecosystem function.

Current Projects:

Gene expression in deep-sea snail symbionts. Hydrothermal vent snails of the genera Ifremeria and Alviniconcha host diverse endosymbiotic bacteria in their gill tissue. These bacteria include sulfide- and methane-oxidizing chemoautotrophs, both of which may provide critical supplies of fixed carbon to the host. As for most symbioses, however, the diverse molecular pathways by which snail symbionts interact with the host, with each other, and with the environment are largely unknown. Our current work uses metatranscriptomics to quantify symbiont gene expression over gradients of environmental substrate availability. This work is coupled to metagenomic analyses to assess symbiont gene content, enabling comparisons with other lineages to better understand how symbiosis affects bacterial genome evolution. This work is a collaboration with Drs. Peter Girguis (Harvard) and Sherry Seston (Alverno College).

Fishes, Lizard Island
Damselfishes, Lizard Island, photo: Danielle Dixson

Reef fish microbiomes. Studies of model organisms have identified critical roles for animal-associated microbiomes as determinants of host development, immunity, and behavior. For most animal lineages, excluding humans, the ecology and evolution of host-associated microbiomes are almost completely unexplored. This is true for the teleost fishes, the largest and most diverse of the vertebrate groups. In collaboration with Dr. Danielle Dixson at the University of Delaware, and funded by generous support from The Simons Foundation (346253 to F.S.), we are characterizing the taxonomic composition and functional gene content of gut microbiomes from coral reef fishes. This work samples across diverse host families, feeding strategies, developmental states, and reef sites (Australia and Belize). Our goals are to better understand the drivers of microbiome structure and to identify patterns that inform manipulative experiments testing the role of the microbiome in fish ecology.

Coral-algae-microbiome interactions. Microbiome communities help mediate interactions between their host and other organisms. We are exploring this hypothesis for diverse species of stony corals in which coral mucus-associated bacteria and archaea may influence interactions between corals and marine algae, including both the micro-algal symbionts (Symbiodinium spp) living in coral tissue, as well as toxic species of macro-algae. This work involves molecular characterizations of microbiome structure coupled with manipulative experiments in the lab and field. This work is driven by collaborations with microbial ecologists (Dr. Koty Sharp, Roger Williams University) and reef community ecologists (Dr. Mark Hay, Georgia Tech), and is funded in part by support from the Teasley Endowment to Georgia Tech, in association with the Aquatic Chemical Ecology Center.

Microbial Genomics and Meta-omics

A holistic understanding of microbial diversity and function requires studies targeting varying levels of biological complexity, from individual cells to entire communities and ecosystems. Advances in DNA sequencing have transformed our capacity to study microorganisms across complexity gradients. Entire genomes can now be sequenced within hours from DNA originating from single cells, facilitating comparative studies of genome architecture and content. Additionally, high-throughput shotgun sequencing can characterize the diverse pool of genes (DNA) and expressed transcripts (RNA) of an entire microbial community (the metagenome and metatranscriptome, respectively).

In combination with single-genome or metagenome analyses, we study microbial community gene expression using high throughout methods (e.g., Illumina technology) to sequence the metatranscriptome of microbial communities. The resulting datasets contain hundreds of thousands to millions of sequence fragments from both the transcriptionally active gene pool and the pool of non-coding RNA molecules. When coupled to metagenome and reference genome data, metatranscriptomic analyses help clarify the link between the genetic potential of a community and its actual functional state (inferred from the transcript pool), reveal novel molecular and ecological adaptations to the geochemical environment, and inform theory about the molecular evolution of highly expressed genes.

This work has focused primarily on bacterioplankton communities, sampled either directly from the marine environment or manipulated within an experimental framework (e.g., via mesocosm or bioreactor treatments). However, we are also applying these methods to other systems, including microbial symbioses as well as to a new project (starting 2016) analyzing the microbial community dynamics and function in various habitats at the Georgia Aquarium.

Analysis of microbial community genomes and transcriptomes typically requires knowledge of both microbiology and informatics. We welcome inquiries from prospective lab members whose interests span these fields.