Evidence for the Ubiquity of Mixotrophic Bacteria in the Upper Ocean: Implications and Consequences

Microorganisms are usually grouped into those relying solely on harvesting light (phototrophy) or those relying solely on the assimilation of organic or inorganic compounds (chemotrophy) to meet their requirements for energy. As a carbon source for biomass production, they can use either inorganic carbon (autotrophy) or organic substances (heterotrophy) (Table ​(Table1).1). Most biogeochemical studies of marine environments use the dichotomy of grouping microorganisms into photo(auto)trophs (primary producers like algae and cyanobacteria) and (organo)heterotrophs (secondary producers, like most heterotrophic bacteria) (see, for example, references 2 and 74). TABLE 1. Definitions of metabolic strategies to obtain carbon and energya It is well known that metabolic modes of aquatic microorganisms are more diverse than that, and modes such as mixotrophy, chemoautotrophy, chemoheterotrophy, or photoheterotrophy do exist. For microeukaryotes, mixotrophy is a widespread phenomenon in aquatic habitats and is observed in many organisms (see, for example, references 16, 62, 82, and 83). Some Bacteria, like purple nonsulfur bacteria (anoxygenic photosynthetic bacteria), are also able to alter between photo-, hetero-, auto-, litho-, and organotrophy, depending on the environmental conditions (93). Although mixotrophic bacteria, which invest in both phototrophic and heterotrophic enzymatic apparatuses and combine them with autotrophic and/or organotrophic strategies, have been isolated from various aquatic environments (see, for example, references 66, 75, and 93), their contribution to total biomass and their importance for biogeochemical processes in aquatic systems have been ignored. However, recent genome data of two Prochlorococcus strains (67) and one Synechococcus strain (56), together with results from isotope tracer uptake experiments (45, 97, 98), suggest that at least certain strains of these ubiquitous picocyanobacteria are not pure photoautotrophs and can take up organic compounds. Cyanobacteria are not the only bacteria that can harvest light energy. Aerobic anoxygenic photosynthetic bacteria (AAnPB) use mainly bacteriochlorophyll a (Bchl-a) for photosynthesis (for example, see references 75 and 93), whereas other bacteria can use proteorhodopsin, a light-driven proton pump (3, 13, 17, 23). Isolated representatives of these bacteria usually use organic carbon for cell synthesis and are characterized as photo(organo)heterotrophs (22-24, 63, 93). Genetic community surveys suggest that AAnPB and proteorhodopsin-containing bacteria (PRB) are common in surface waters throughout the oceans of the world and can make up a substantial fraction of the bacterial community in oligotrophic marine environments (see, for example, references 3-5, 10, 34, 35, 69-72, 80, and 89). Furthermore, it has been shown that phylogenetic clades, including organisms with photoreceptors, can be significant in degradation processes of organic compounds (43-45). These observations suggest that mixotrophic bacteria may be major players in photo-, hetero-, auto-, and organotrophic processes in the upper ocean, which may demand a thorough revision of our understanding of how microorganisms contribute to biogeochemical cycles in the marine environment.