Phage Community Dynamics in Hot Springs

Abstract

In extreme thermal environments such as hot springs, phages are the only known microbial predators. Here we present the first study of prokaryotic and phage community dynamics in these environments. Phages were abundant in hot springs, reaching concentrations of a million viruses per milliliter. Hot spring phage particles were resistant to shifts to lower temperatures, possibly facilitating DNA transfer out of these extreme environments. The phages were actively produced, with a population turnover time of 1 to 2 days. Phage-mediated microbial mortality was significant, making phage lysis an important component of hot spring microbial food webs. Together, these results show that phages exert an important influence on microbial community structure and energy flow in extreme thermal environments.Phages, viruses that infect and kill bacteria, are important components of all known microbial food webs. The influences of phages on ecosystem dynamics are best understood in the context of the marine microbial food web, the consortium of heterotrophic and autotrophic prokaryotes, as well as their predators that inhabit the Earth's oceans and seas. The marine microbial food web regulates the transfer of energy and nutrients to higher trophic levels and greatly influences global carbon and nutrient cycles (6,32,43). Heterotrophic production by prokaryotes within the marine microbial food web accounts for Ϸ50% of the oceanic carbon fixed by photosynthesis every day (5). These heterotrophs, in turn, are controlled in a top-down fashion by protozoa and phages (23,44). Phages are also important mediators of genetic exchange in the environment via generalized (29, 41, 42) and specialized (1, 21, 50) transduction.In extreme thermal environments above the upper temperature limit for eukaryotic life, phages are the only known predators of prokaryotes. Despite their potential importance, very little is known about the influences of phages on the microbial communities in these ecosystems. Phage particles in hot springs have been observed by electron microscopy (40), and phages have been cultured on Bacteria and Archaea isolated from these ecosystems (4,8,17,35,39,45,46,(56)(57)(58). However, no effort has been made to determine the abundance or dynamics of naturally occurring phage communities or to quantify the effects of these phages on the microbial populations in extreme thermal environments.Here we show that phages are abundant and active components of hot springs capable of killing a significant proportion of the resident microbial populations. In addition, the resistance of the phage particles to temperature shifts implies that phages can laterally transfer DNA from these extreme environments. MATERIALS AND METHODSDirect counts of prokaryotes and VLP. Prokaryotes (Bacteria and Archaea) and virus-like particles (VLP) were counted by filtering samples fixed in 2% paraformaldehyde onto a 0.02-m Anodisc (Whatman), staining with SYBR Gold (Molecular Probes, Inc.), and direct counting by epifluorescent microscopy (37). Direct count...

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