Cooperative motility, force generation and mechanosensing in a foraging non-photosynthetic diatom

Diatoms are ancestrally photosynthetic microalgae. However, some underwent a major evolutionary transition, losing photosynthesis to become obligate heterotrophs. The molecular and physiological basis for this transition is unclear. Here, we isolate and characterize new strains of non-photosynthetic...

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Main Authors: Peng Zheng, Kayo Kumadaki, Christopher Quek, Zeng Hao Lim, Yonatan Ashenafi, Zhi Ting Yip, Jay Newby, Andrew J. Alverson, Yan Jie, Gregory Jedd
Format: Article
Language:English
Published: The Royal Society 2023-10-01
Series:Open Biology
Subjects:
Online Access:https://royalsocietypublishing.org/doi/10.1098/rsob.230148
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author Peng Zheng
Kayo Kumadaki
Christopher Quek
Zeng Hao Lim
Yonatan Ashenafi
Zhi Ting Yip
Jay Newby
Andrew J. Alverson
Yan Jie
Gregory Jedd
author_facet Peng Zheng
Kayo Kumadaki
Christopher Quek
Zeng Hao Lim
Yonatan Ashenafi
Zhi Ting Yip
Jay Newby
Andrew J. Alverson
Yan Jie
Gregory Jedd
author_sort Peng Zheng
collection DOAJ
description Diatoms are ancestrally photosynthetic microalgae. However, some underwent a major evolutionary transition, losing photosynthesis to become obligate heterotrophs. The molecular and physiological basis for this transition is unclear. Here, we isolate and characterize new strains of non-photosynthetic diatoms from the coastal waters of Singapore. These diatoms occupy diverse ecological niches and display glucose-mediated catabolite repression, a classical feature of bacterial and fungal heterotrophs. Live-cell imaging reveals deposition of secreted extracellular polymeric substance (EPS). Diatoms moving on pre-existing EPS trails (runners) move faster than those laying new trails (blazers). This leads to cell-to-cell coupling where runners can push blazers to make them move faster. Calibrated micropipettes measure substantial single-cell pushing forces, which are consistent with high-order myosin motor cooperativity. Collisions that impede forward motion induce reversal, revealing navigation-related force sensing. Together, these data identify aspects of metabolism and motility that are likely to promote and underpin diatom heterotrophy.
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spelling doaj.art-c6d48d3a7cfd46258d10d7034f0d265b2023-10-03T23:05:17ZengThe Royal SocietyOpen Biology2046-24412023-10-01131010.1098/rsob.230148Cooperative motility, force generation and mechanosensing in a foraging non-photosynthetic diatomPeng Zheng0Kayo Kumadaki1Christopher Quek2Zeng Hao Lim3Yonatan Ashenafi4Zhi Ting Yip5Jay Newby6Andrew J. Alverson7Yan Jie8Gregory Jedd9Temasek Life Sciences Laboratory, 117604 SingaporeDepartment of Physics, National University of Singapore, 117542 SingaporeTemasek Life Sciences Laboratory, 117604 SingaporeTemasek Life Sciences Laboratory, 117604 SingaporeDepartment of Mathematical and Statistical Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2G1Department of Biological Sciences, National University of Singapore, 117543 Singapore, SingaporeDepartment of Mathematical and Statistical Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2G1Department of Biological Sciences, University of Arkansas, SCEN 601, Fayetteville, AR 72701, USADepartment of Physics, National University of Singapore, 117542 SingaporeTemasek Life Sciences Laboratory, 117604 SingaporeDiatoms are ancestrally photosynthetic microalgae. However, some underwent a major evolutionary transition, losing photosynthesis to become obligate heterotrophs. The molecular and physiological basis for this transition is unclear. Here, we isolate and characterize new strains of non-photosynthetic diatoms from the coastal waters of Singapore. These diatoms occupy diverse ecological niches and display glucose-mediated catabolite repression, a classical feature of bacterial and fungal heterotrophs. Live-cell imaging reveals deposition of secreted extracellular polymeric substance (EPS). Diatoms moving on pre-existing EPS trails (runners) move faster than those laying new trails (blazers). This leads to cell-to-cell coupling where runners can push blazers to make them move faster. Calibrated micropipettes measure substantial single-cell pushing forces, which are consistent with high-order myosin motor cooperativity. Collisions that impede forward motion induce reversal, revealing navigation-related force sensing. Together, these data identify aspects of metabolism and motility that are likely to promote and underpin diatom heterotrophy.https://royalsocietypublishing.org/doi/10.1098/rsob.230148non-photosynthetic diatomheterotrophygliding motilitymechanosensingforce generation
spellingShingle Peng Zheng
Kayo Kumadaki
Christopher Quek
Zeng Hao Lim
Yonatan Ashenafi
Zhi Ting Yip
Jay Newby
Andrew J. Alverson
Yan Jie
Gregory Jedd
Cooperative motility, force generation and mechanosensing in a foraging non-photosynthetic diatom
Open Biology
non-photosynthetic diatom
heterotrophy
gliding motility
mechanosensing
force generation
title Cooperative motility, force generation and mechanosensing in a foraging non-photosynthetic diatom
title_full Cooperative motility, force generation and mechanosensing in a foraging non-photosynthetic diatom
title_fullStr Cooperative motility, force generation and mechanosensing in a foraging non-photosynthetic diatom
title_full_unstemmed Cooperative motility, force generation and mechanosensing in a foraging non-photosynthetic diatom
title_short Cooperative motility, force generation and mechanosensing in a foraging non-photosynthetic diatom
title_sort cooperative motility force generation and mechanosensing in a foraging non photosynthetic diatom
topic non-photosynthetic diatom
heterotrophy
gliding motility
mechanosensing
force generation
url https://royalsocietypublishing.org/doi/10.1098/rsob.230148
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