Bimodal occupancy-frequency distributions uncover the importance of regional dynamics in shaping marine microbial biogeography
Authors: Lindh Markus V. , Sjöstedt Johanna , Ekstam Börje , Casini Michele , Lundin Daniel , Hugerth Luisa W. , Hu Yue O. O. , Andersson Anders F. , Andersson Agneta , Legrand Catherine , Pinhassi Jarone 
Published: February 2016

Metapopulation theory developed in terrestrial ecology provides applicable frameworks for interpreting the role of local and regional processes in shaping species distribution patterns. Yet, empirical testing of metapopulation models on microbial communities is essentially lacking. Here we determined regional bacterioplankton dynamics from monthly transect sampling in the Baltic Sea Proper (16 sites, 11 occasions, 2010-2011) using 16S rRNA gene pyrosequencing. A strong positive correlation was found between local relative abundance and occupancy of populations. Notably, the occupancy-frequency distributions (the number of populations occupying different number of sites) were significantly bimodal with a satellite mode of mostly rare endemic populations and a core mode of abundant cosmopolitan populations (e.g.Synechococcus, SAR11 and SAR86 clade members). Observed temporal changes in population distributions supported theoretical predictions that stochastic variation in local extinction and colonization rates accounted for observed bimodality. Moreover, bimodality was found for bacterioplankton across the entire Baltic Sea, and was also frequent in globally distributed datasets where average Bray-Curtis distances were significantly different between bimodal and non-bimodal datasets. Still, datasets spanning waters with distinct physicochemical characteristics or environmental gradients, e.g. brackish and marine or surface to deep waters, typically lacked significant bimodal patterns. When such datasets were divided into subsets with coherent environmental conditions, bimodal patterns emerged, highlighting the importance of positive feedbacks between local abundance and occupancy within specific biomes. Thus, metapopulation theory applied to microbial biogeography can provide novel insights into the mechanisms governing shifts in biodiversity resulting from natural or anthropogenically induced changes in the environment.

Significance statement

Marine bacteria regulate global cycles of elements essential to life and respond rapidly to environmental change. Yet, the ecological factors that determine distribution and activity patterns of microbial populations across different spatial scales and environmental gradients remain basically unconstrained. Our metapopulation model-based analyses show that dispersal-driven processes contribute to structuring the biogeography of marine microorganisms from small to large geographical areas. Discovery of bimodal distribution patterns pinpointed satellite microbial populations with highly restricted ranges and defined abundant core populations widely distributed in coherence with environmental conditions. Thus, application of metapopulation models on microbial community structure may allow the definition of biogeographic regions critical for interpreting the outcome of future ocean changes.

Classification

Biological Sciences, Environmental Sciences