Abundance determines the functional role of bacterial phylotypes in complex communities

Abstract

Bacterial communities are essential for the functioning of the Earth’s ecosystems1. A key challenge is to quantify the functional roles of bacterial taxa in nature to understand how the properties of ecosystems change over time or under different environmental conditions2. Such knowledge could be used, for example, to understand how bacteria modulate biogeochemical cycles3, and to engineer bacterial communities to optimize desirable functional processes4. Communities of bacteria are, however, extraordinarily complex with hundreds of interacting taxa in every gram of soil and every millilitre of pond water5. Little is known about how the tangled interactions within natural bacterial communities mediate ecosystem functioning, but high levels of bacterial diversity have led to the assumption that many taxa are functionally redundant6. Here, we pinpoint the bacterial taxa associated with keystone functional roles, and show that rare and common bacteria are implicated in fundamentally different types of ecosystem functioning. By growing hundreds of bacterial communities collected from a natural aquatic environment (rainwater-filled tree holes) under the same environmental conditions, we show that negative statistical interactions among abundant phylotypes drive variation in broad functional measures (respiration, metabolic potential, cell yield), whereas positive interactions between rare phylotypes influence narrow functional measures (the capacity of the communities to degrade specific substrates). The results alter our understanding of bacterial ecology by demonstrating that unique components of complex communities are associated with different types of ecosystem functioning.