Unconventional cell division cycles from marine-derived yeasts

Abstract

Fungi have been found in every marine habitat that has been explored, however, the diversity and functions of fungi in the ocean are poorly understood. In this study, fungi were cultured from the marine environment in the vicinity of Woods Hole, MA, USA including from plankton, sponge and coral. Our sampling resulted in 36 unique species across 20 genera. We observed many isolates by time-lapse differential interference contrast (DIC) microscopy and analyzed modes of growth and division. Several black yeasts displayed highly unconventional cell division cycles compared to those of traditional model yeast systems. Black yeasts have been found in habitats inhospitable to other life and are known for halotolerance, virulence, and stress-resistance. We find that this group of yeasts also shows remarkable plasticity in terms of cell size control, modes of cell division, and cell polarity. Unexpected behaviors include division through a combination of fission and budding, production of multiple simultaneous buds, and cell division by sequential orthogonal septations. These marine-derived yeasts reveal alternative mechanisms for cell division cycles that seem likely to expand the repertoire of rules established from classic model system yeasts.

Diversity and biomass dynamics of unicellular marine fungi during a spring phytoplankton bloom

“…In laboratory cultures, doubling times as short as 100 min have been shown for typical budding yeasts (Slater et al, 1977). However, Mitchison-Field et al (2019) recently identified new division forms in marine isolates, such as spherical division, multiple budding, or readily transitioning between both in a single generation; allowing for a single mother cell to generate several daughter cells at once. These findings highlight our currently limited knowledge on marine yeast ecology and the need for modern microscopy-based techniques, such as the CARD-FISH protocol presented here, to be incorporated into environmental surveys.…”

Growth and division mode plasticity is dependent on cell density in marine-derived black yeasts

“…There were considerable differences between the current collection at Sugashima and what was identified around Woods Hole (Mitchison-Field et al, 2019) (Table 2, *1). Only seven species were isolated in both studies (Aureobasidium pullulans, Cladosporium cladosporioides, Cladosporium halotolerans, Hortaea werneckii, Metschnikowia bicuspidate, Meyerozyma guilliermondii, and Parengyodontium album).…”

“…The species were identified via DNA barcode sequencing, and the division pattern was observed for budding and black yeasts (no fission yeast was isolated). The collected species, or even genera, only partially overlapped with those identified by (Mitchison-Field et al, 2019), suggesting the existence of highly divergent fungal species in the ocean. Surprisingly, the division pattern of black yeasts (H. werneckii, A. pullulans, and other unidentified species) was initially inconsistent with those previously reported in (Mitchison-Field et al, 2019), and this enigma was solved through the observation of cell density-dependent alterations in their division patterns.…”

“…The remaining three fungi that formed yeast-like colonies produced black or brown pigment. Two of them have been extensively studied by (Mitchison-Field et al, 2019): A. pullulans (Fig. 4A) and H. werneckii (Fig.…”

“…In this study, inspired by (Mitchison-Field et al, 2019), free-living marine fungi were collected in front of Nagoya University's Marine Biological Laboratory (NU-MBL) on Sugashima Island, Toba, Japan (Fig. 1A).…”