Eco-Evolutionary Perspectives on Mixoplankton

Abstract

Mixotrophy, i.e., the capability of both phototrophy and phagotrophy within a single organism, is a prominent trophic mode in aquatic ecosystems. Mixotrophic strategies can be highly advantageous when feeding or photosynthesis alone does not sustain metabolic needs. In the current review, we discuss the functional types of mixotrophic marine protists (herein mixoplankton) within the context of evolution. Permanent plastids have been established in large due to gene transfer from prey and/or endosymbionts to the host cell. In some kleptoplastidic mixoplankton, prior gene transfers and active transcription of plastid related genes in the host can help maintain and extend retention of the current kleptoplast. In addition to kleptoplasts, the prey nucleus is also sometimes retained and actively transcribed to help maintain and even replicate the kleptoplasts. Endosymbiotic relations vary considerably in the extent to which hosts affect symbionts. For example, some endosymbionts are heavily modified to increase photosynthetic efficiency, or are controlled in their cell division. It can be proposed that many kleptoplasts and endosymbionts are in fact en route to becoming permanent plastids. Conditions such as increased temperature and limiting nutrients seem to favor phagotrophy in mixoplankton. However, responses of mixoplankton to changing environmental conditions like light irradiance, temperature, nutrient, and prey availability are variable and species-specific. Studying mixotrophs with temporary plastids could elucidate past and future evolutionary mechanisms and dynamics of processes such as phagotrophy and the establishment of (secondary) permanent plastids.

Retention of Prey Genetic Material by the Kleptoplastidic Ciliate Strombidium cf. basimorphum

“…All these processes argue for an active transcription of at least partially remained nuclei of the prey. These results will deserve further and extensive studies to elucidate the responses of the host toward functions related to the kleptoplasts (Uzuka et al, 2019) and the presence of photosynthesis-related genes (and eventually their evolutionary origin) within the genome of the host (Hongo et al, 2019;Hehenberger et al, 2019;Mansour and Anestis, 2021).…”

Micromonas, a small pigmented flagellate, predominates the nanoflagellate and photosynthetic picoeukaryote communities in the northern South China Sea

“…For example, a general trend of an increased phagotrophic strategy with increased temperature was commonly found in PNFs (Mansour & Anestis, 2021). Moreover, the condition of high irradiance combined with inorganic nutrient limitation was observed to stimulate phagotrophy in many pigmented flagellates (Mansour & Anestis, 2021;Stoecker et al, 2017). Some Chrysophyte species were found to grow in darkness if bacteria presented as prey, while their phototrophic modes triggered as a survival strategy in the absence of abundant prey (Stoecker et al, 2017).…”

“…Mixotrophic strategies give Xin Guo and Mengwen Pang shared equally to first authorship. competitive advantages to different mixotrophs relative to their strict auto-and hetero-trophic competitors when a single nutritional mode does not fulfil cellular nutrient requirements (Leles et al, 2018;Mansour & Anestis, 2021). As an organism's ability to use alternative forms of nutrition, mixotrophy plays an important role in the energy budgets and biogeochemical cycling in planktonic ecosystems (Stoecker et al, 2017).…”

“…Studies have found that MNFs make up a large proportion of PNFs, for example, about 50% in the Sargasso Sea (Arenovski et al, 1995 ) and the NW Mediterranean (Unrein et al, 2014 ), 5%–10% in the Ross Sea (Moorthi et al, 2009 ), 2%–29% in a coastal upwelling area in Chile (Vargas et al, 2012 ) and 5%–36% in the Tara Oceans project (Li et al, 2022 ), significantly impact bacterioplankton dynamics via grazing (Stoecker et al, 2017 ). Mixotrophic strategies give competitive advantages to different mixotrophs relative to their strict auto‐ and hetero‐trophic competitors when a single nutritional mode does not fulfil cellular nutrient requirements (Leles et al, 2018 ; Mansour & Anestis, 2021 ). As an organism's ability to use alternative forms of nutrition, mixotrophy plays an important role in the energy budgets and biogeochemical cycling in planktonic ecosystems (Stoecker et al, 2017 ).…”

Lack of mixotrophy in three Karenia species and the prey spectrum of Karenia mikimotoi (Gymnodiniales, Dinophyceae)

“…was incubated at 20°C under the a photosynthetic organism is fundamental for predicting its population dynamics and bloom formation in marine ecosystems (Jeong et al 2015). Furthermore, determination of the presence or lack of mixotrophic ability and prey items has greatly improved our understanding of evolution in photosynthetic organisms (Jones 2000, Mansour andAnestis 2021). Therefore, exploring the mixotrophic ability of an organism is a crucial step regarding its ecology and evolution.…”