The Atmosphere: Its Developmental History and Contributions to Microbial Evolution and Habitat

TERRY J. HENDERSON AND HARRY SALEM

Research and Technology Directorate, US Army Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD 21010- 5424, USA E-mail: terry.j.henderson.civ@mail.mil,harry.salem.civ@mail.mil

1.1 Introduction

Research efforts focused on the Earth's biota have been limited almost exclusively to land, soil and aquatic habitats; however, this focus is now beginning to change. There is a renewed and building interest in the ecology of living microorganisms found in the atmosphere. Hundreds of thousands of individual microorganisms can exist in a cubic meter of air, which can represent hundreds of different taxa. The atmosphere is one of our Planet's most intriguing habitats to investigate because extreme cold temperatures, hypobaria (low pressures), desiccation and ultraviolet (UV) irradiation make it more indicative of the surface conditions on Mars rather than anywhere else on Earth. In a recent report, the atmosphere was described as "one of the last frontiers of biological exploration on Earth."

The Planet's atmospheric biota, however, remains one of the most challenging to investigate, which has been reflected by the many shortcomings encountered throughout the history of aerobiology. In the past, aerobiological studies relied almost exclusively on culture-based analyses that neglected the vast majority of microbes present in air samples. This is because only 0.1-10% of the total airborne microbial flora are able to grow in culture. Airborne microorganisms can also become damaged or killed by desiccation, UV irradiation or the extreme low temperatures that occur in the atmosphere. Acquiring culture-independent microbiological data, on the other hand, can be difficult because the density of airborne microorganisms decreases with increasing altitude.' Large, or sometimes enormous, volumes of air must be collected and processed for detecting microorganisms with molecular detection assays and air-sampling systems must also be designed to prevent cell trauma and damage and sample contamination. To complicate matters, a modern, standard method for reading and scoring microorganisms in aerobiological samples does not exist, making the interpretation and inter-comparison of results difficult. Finally, studies of atmospheric residence times (the lifetime of particles aloft in the atmosphere) for microorganisms and their dispersal patterns rely on computer simulations based on theoretical mathematical models that are difficult to correlate with experimental data. Such experimental design and engineering challenges explain why the upper atmosphere is one of the least explored biological environments on Earth, rivaling deep oceanic and subsurface environments.

Given the renewed interest in aerobiology and the inherent difficulties in aerobiological research, it should be of no surprise that the field is characterized by a remarkable lack of knowledge and a great deal of speculation. Some of the most important and fundamental questions regarding microorganisms in the atmosphere cannot be answered definitively and are active topics of debate. Undoubtedly, one of the more fundamental questions concerns the contributions of the atmosphere to the origin and evolution of microbial life. A complete account of this topic should include the evolutionary history of airborne microorganisms, the details of which have never been addressed to date. Another question central to aerobiology is whether the atmosphere can be considered a true habitat for airborne microorganisms. Several recent reports allude to the atmosphere as a habitat or ecosystem, especially in the case of microorganisms,' but others argue that the debate is far from settled' and subscribe to the more traditional point of view that the atmosphere is merely a conduit for dispersing microbes to distant locations. Other important problems in aerobiology have somewhat vague and tenuous answers simply because they are difficult to answer by experimentation. For microorganisms in particular, the most fundamental of these concern deriving realistic values for atmospheric residence times and understanding cosmopolitan dispersal by atmospheric transport (see, for example, Frohlich-Nowoisky et al., Wilkinson et al. or Smith et al.). Atmospheric air is the primary medium for dispersing microorganisms across the globe and connecting all microbial habitats on the Earth's surface, but it is not known whether the atmosphere contains biogeographic regions similar to those found on the Planet's surface.' We discuss the most recent research focused on establishing more concrete answers to these questions and, when appropriate, present our own speculation. Because the developmental history of the atmosphere is intimately related to microbial evolution and because some understanding of atmospheric structure is necessary to discuss aerobiology in detail, we begin by outlining this history and the Earth's present-day atmosphere.

1.2 The Origin and Evolution of the Earth's Atmosphere

The processes by which the current atmosphere arose from earlier conditions are exceedingly complex; however, evidence related to these processes, although indirect, is abundant. Ancient sediments and rocks record the past changes in the atmospheric composition from chemical...